CeilingFan and Mugiwara are novel lytic siphoviruses isolated from soil. CeilingFan was isolated using Streptomyces griseus ATCC 10137, and it has a genome size of 132,946 bp. Mugiwara was isolated using Streptomyces avermitilis NRRL 8165, and its genome size is 133,330 bp. Both phages are assigned to the BE2 cluster of actinobacteriophages based on gene content similarity.
","acknowledgements":"
We thank members of the Howard Hughes Medical Institute Science Education Alliance-Phage Hunters Advancing Genomics and Evolutionary Science (SEA-PHAGES) program and Manuscript Data Interpretation and Nomenclature Review Team (MINT) for their support and review of the manuscript. We acknowledge Daniel French, Makayla Gomperts, and Mirkhon Normurodo at the University of Evansville who took part in the isolation of CeilingFan and University of Ottawa for isolating Mugiwara as part of their participation in the SEA-PHAGES program.
","authors":[{"affiliations":["University of Lagos, Lagos, Nigeria"],"departments":["Department of Microbiology"],"credit":["investigation","supervision","project","validation","writing_originalDraft","writing_reviewEditing"],"email":"insa@unilag.edu.ng","firstName":"Imade Y.","lastName":"Nsa ","submittingAuthor":true,"correspondingAuthor":true,"equalContribution":false,"WBId":null,"orcid":"https://orcid.org/0000-0001-5606-268X"},{"affiliations":["University of Lagos, Lagos, Nigeria"],"departments":["Department of Microbiology"],"credit":["investigation","writing_originalDraft","writing_reviewEditing"],"email":"eziejiofor@gmail.com","firstName":"Ezichukwu E.","lastName":"Ejiofor","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":false,"WBId":null,"orcid":null},{"affiliations":["University of Lagos, Lagos, Nigeria"],"departments":["Department of Microbiology"],"credit":["investigation","writing_originalDraft","writing_reviewEditing"],"email":"ajayiemmanuel630@gmail.com","firstName":"Emmanuel T. ","lastName":"Ajayi","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":false,"WBId":null,"orcid":null},{"affiliations":["University of Lagos, Lagos, Nigeria"],"departments":["Department of Microbiology"],"credit":["investigation","writing_originalDraft","writing_reviewEditing"],"email":"okoliifunanya497@gmail.com","firstName":"Ifunanya O. ","lastName":"Okoli","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":false,"WBId":null,"orcid":null},{"affiliations":["University of Lagos, Lagos, Nigeria"],"departments":["Department of Microbiology"],"credit":["investigation","writing_originalDraft","writing_reviewEditing"],"email":"xavierchibueze@gmail.com","firstName":"Chibueze S. ","lastName":"Uchegbu","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":false,"WBId":null,"orcid":null},{"affiliations":["University of Lagos, Lagos, Nigeria"],"departments":["Department of Microbiology"],"credit":["investigation","writing_originalDraft","writing_reviewEditing"],"email":"opeoluwaaaa@gmail.com","firstName":"Opeoluwa S. ","lastName":"Aworetan","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":true,"WBId":null,"orcid":null},{"affiliations":["University of Lagos, Lagos, Nigeria"],"departments":["Department of Microbiology"],"credit":["investigation","writing_originalDraft","writing_reviewEditing"],"email":"jebfuad@gmail.com","firstName":"Fuad T.","lastName":" Jebe-Abdullah","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":true,"WBId":null,"orcid":null},{"affiliations":["University of Lagos, Lagos, Nigeria"],"departments":["Department of Microbiology"],"credit":["investigation","writing_originalDraft","writing_reviewEditing"],"email":"hauwajkam12@gmail.com","firstName":"Hauwa J.","lastName":" Kamselem","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":true,"WBId":null,"orcid":null},{"affiliations":["University of Lagos, Lagos, Nigeria"],"departments":["Department of Microbiology"],"credit":["investigation","writing_originalDraft","writing_reviewEditing"],"email":"oluwashinaabidoye@yahoo.com","firstName":"Shina O.","lastName":" Abidoye","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":true,"WBId":null,"orcid":null},{"affiliations":["University of Lagos, Lagos, Nigeria"],"departments":["Department of Microbiology"],"credit":["investigation","writing_originalDraft","writing_reviewEditing"],"email":"evansoleka6@gmail.com","firstName":"Evans C. ","lastName":"Oleka","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":true,"WBId":null,"orcid":null},{"affiliations":["University of Lagos, Lagos, Nigeria"],"departments":["Department of Microbiology"],"credit":["investigation","writing_originalDraft","writing_reviewEditing"],"email":"oluwatunkunmi@gmail.com","firstName":"Oluwatunkunmi J. ","lastName":"Okupa","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":true,"WBId":null,"orcid":null},{"affiliations":["University of Lagos, Lagos, Nigeria"],"departments":["Department of Microbiology"],"credit":["investigation","writing_originalDraft","writing_reviewEditing"],"email":"lawalfuhad51@gmail.com","firstName":"Fuhad T.","lastName":"Lawal","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":true,"WBId":null,"orcid":null},{"affiliations":["University of Lagos, Lagos, Nigeria"],"departments":["Department of Microbiology"],"credit":["investigation","writing_originalDraft","writing_reviewEditing"],"email":"immanuelgrace.o@gmail.com","firstName":"Grace O. ","lastName":"Immanuel","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":true,"WBId":null,"orcid":null},{"affiliations":["University of Lagos, Lagos, Nigeria"],"departments":["Department of Microbiology"],"credit":["investigation","writing_originalDraft","writing_reviewEditing"],"email":"emmanueltomi3264@gmail.com","firstName":"Tomi E.","lastName":"Adeyanju","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":true,"WBId":null,"orcid":null},{"affiliations":["University of Lagos, Lagos, Nigeria"],"departments":["Department of Microbiology"],"credit":["investigation","writing_originalDraft","writing_reviewEditing"],"email":"onyekachifaith0804@gmail.com","firstName":"Faith O. ","lastName":"Onyekachi","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":true,"WBId":null,"orcid":null},{"affiliations":["University of Lagos, Lagos, Nigeria"],"departments":["Department of Microbiology"],"credit":["investigation","writing_originalDraft","writing_reviewEditing"],"email":"gloriaakpederi5@gmail.com","firstName":"Omogwigho G. ","lastName":"Akpederi","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":true,"WBId":null,"orcid":null},{"affiliations":["University of Lagos, Lagos, Nigeria"],"departments":["Department of Microbiology"],"credit":["investigation","writing_originalDraft","writing_reviewEditing"],"email":"foyinsolaj@gmail.com","firstName":"Oluwafoyinsolami I. ","lastName":"Adisa","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":true,"WBId":null,"orcid":null},{"affiliations":["University of Lagos, Lagos, Nigeria"],"departments":["Department of Microbiology"],"credit":["investigation","writing_originalDraft","writing_reviewEditing"],"email":"midexy24@gmail.com","firstName":"Modesola O. ","lastName":"Onikoro","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":true,"WBId":null,"orcid":null},{"affiliations":["University of Evansville, Evansville, Indiana, United States"],"departments":["Department of Biology"],"credit":["investigation","writing_originalDraft","writing_reviewEditing"],"email":"cb508@evansville.edu","firstName":"Chase ","lastName":"Boyles","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":false,"WBId":null,"orcid":null},{"affiliations":["University of Evansville, Evansville, Indiana, United States"],"departments":["Department of Biology"],"credit":["investigation","supervision","validation","writing_originalDraft","writing_reviewEditing"],"email":"jm757@evansville.edu","firstName":"Julie A.","lastName":"Merkel","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":false,"WBId":null,"orcid":null},{"affiliations":["University of Lagos, Lagos, Nigeria"],"departments":["Department of Microbiology"],"credit":["investigation","supervision","writing_originalDraft","writing_reviewEditing"],"email":"milori@unilag.edu.ng","firstName":"Matthew O. ","lastName":"Ilori","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":false,"WBId":null,"orcid":null}],"awards":[],"conflictsOfInterest":null,"dataTable":null,"extendedData":[],"funding":"No funding was received to assist with the preparation of this manuscript.
","image":{"url":"https://portal.micropublication.org/uploads/5ca00a0f83bf46e49824dad5e0f6c07a.png"},"imageCaption":"(A) Plaques formed by phage CeilingFan on S. griseus ATCC 10137. (B) Plaques formed by phage Mugiwara on S. avermitilis NRRL 8165. (C) Transmission electron micrograph of Mugiwara stained with 1% uranyl acetate and imaged at 120 kV, Scale bar = 75 nm. (D) Transmission electron micrograph (TEM) of CeilingFan stained with 1% uranyl acetate and imaged at 100 kV, Scale bar = 100 nm.
","imageTitle":"Plaque pictures and transmission electron micrographs of CeilingFan and Mugiwara
","methods":"","reagents":"","patternDescription":"The continued discovery and characterization of Streptomyces bacteriophages improve our understanding of phage-host interactions, phage diversity, phage genome architecture, and their potential applications in combating antibiotic resistance. Streptomyces griseus subsp. griseus ATCC 10137 and Streptomyces avermitilis NRRL 8165 are bacterial type strains for studying the biology of Streptomyces (Hatfull, 2020; Kronheim et al., 2023; Rackow et al., 2024).
Here, we report the characteristics of CeilingFan and Mugiwara, isolated from slightly damp soil in Evansville, IN, USA (37.973088 N, 87.533631 W) and a grassy area near fir trees in Noertrange, Luxembourg (49.98127, 5.903158 E), respectively. Using standard protocols (Zorawik et al., 2024), CeilingFan was extracted by the enrichment method and Mugiwara by direct isolation. Briefly, soil samples were suspended in nutrient broth supplemented with glucose, MgCl2, and Ca (NO3)2, and the suspension was subsequently filtered using a 0.22 µm filter. The filtrate for Mugiwara was plated directly in top agar supplemented with S. avermitilis NRRL 8165, whereas the filtrate for CeilingFan was first inoculated with S. griseus ATCC 10137, incubated at 20 °C for 72h, and the resulting culture filtered before the filtrate was plated in top agar with S. griseus ATCC 10137. Plates for Mugiwara and CeilingFan were always incubated at 37 ˚C and 30 ˚C, respectively. Mugiwara formed small, clear plaques, whereas CeilingFan formed slightly larger, clear plaques. Both phages were purified through three rounds of plating before lysates were prepared. Transmission electron microscopy after negative staining of lysates with uranyl acetate (1%) revealed siphovirus morphology for both phages. CeilingFan has a capsid diameter of 62 nm and a tail length of 346 nm, while Mugiwara featured a larger capsid measuring 79 nm and a tail length of 348 nm (Figure 1, n=1).
DNA was extracted from high-titer lysates of CeilingFan and Mugiwara using the Promega Wizard DNA Cleanup kit. CeilingFan and Mugiwara genomes were prepared for sequencing using the NEB Ultra II Library kit (New England Biolabs, Ipswich, MA, USA) and sequenced on the Illumina MiSeq 1000 v3 platform using the 150-bp single-end sequencing strategy at the Pittsburgh Bacteriophage Institute. Raw reads were assembled using Newbler version v3.0 (Miller et al., 2010) and checked for completeness and genomic termini using Consed v29 (Gordon et al., 1998; Russell, 2018). The number of reads generated for CeilingFan was 413,717, allowing for assembly with 466-fold coverage of a genome 132,946 bp long, with G+C content of 49.3% and a direct terminal repeat length of 12,339 bp. For Mugiwara, 342,705 reads provided 391-fold coverage of an assembled genome 133,330 bp long with G+C content of 49.1% and a direct terminal repeat length of 11,945 bp.
Auto-annotation was performed in DNA Master v5.23.6 (http://cobamide2.bio.pitt.edu/) with Glimmer v3.02 (Delcher et al., 2007) and Genemark v2.5 (Besemer and Borodovsky, 2005), then manually refined using Starterator (http://phages.wustl.edu/starterator) for start sites comparisons (Pope and Jacobs-Sera, 2018). Functions were predicted by BLAST, using the Actinobacteriophage and NCBI non-redundant database searches v2.13.0 (Altschul et al., 1997; Russell and Hatfull, 2017), HHPRED, using the PDB_mmCIF70, (Söding, 2005), Pfam- v.36, NCBI Conserved Domains databases, Phamerator, using Actino_draft database v578 (Cresawn et al., 2011). The presence of tRNAs and tmRNAs were examined using Aragorn v1.2.41 (Laslett and Canbett, 2004) and tRNAscan-SE v2.0.12 (Lowe and Eddy, 1999) and membrane proteins were identified using SOSUI v1.1 (Hirokawa et al., 1998; Mitaku & Hirokawa, 1999; Mitaku et al., 2002) and DeepTMHMM 1.0.42 (Hallgren et al., 2022). All software were used with default parameters.
Based on gene content similarity (GCS) of at least 35% to previously annotated phages within the Actinobacteriophage Database (phagesdb.org), both phages were assigned to subcluster BE2 (Russell and Hatfull, 2017; Pope et. al., 2017) and share 79% GCS with one another. CeilingFan encodes 44 predicted tRNAs, one predicted tmRNA and 248 predicted protein-coding genes, with 64 of the latter assigned putative functions. Mugiwara similarly encodes 44 putative tRNAs and one tmRNA and has 247 predicted protein-coding genes, of which 59 could be assigned putative functions.
As is typical for BE2 phages, holin and endolysin functions could be identified while no integrase or immunity repressors could be identified, the latter suggesting these phages are unlikely to establish lysogeny. MazG-like nucleotide, Ro-like RNA binding protein, DprA-like ssDNA binding protein, Cas4 exonuclease were among the functions conserved across BE2 PHAGES. Mugiwara lacks the Lys-M-like peptidoglycan binding protein found in a majority of BE2 phages (23/33 phages) but it is the only BE2 member in which a putative histidine triad nucleotide binding protein has been identified. Uniquely, Mugiwara encodes a putative thioredoxin that shares little homology to the thioredoxin encoded by other BE2 phages. Similarly, CeilingFan encodes an HNH endonuclease and DNA Q-like DNA polymerase III subunit with little homology to that encoded by other BE2 phages, except for phage TomSawyer.
Nucleotide sequence accession numbers
The complete genome sequences for both phages are available at GenBank with Accession Nos. PV165877 and PV876970 and Sequence Read Archive (SRA) Nos.SRR34858420 and SRR34858425 (CeilingFan and Mugiwara respectively).
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","pubmedId":"","doi":"10.1007/978-1-0716-3798-2_17 PMID: 38526736"}],"title":"Genome Sequences of Streptomyces Cluster BE2 phages CeilingFan and Mugiwara
","reviews":[{"reviewer":{"displayName":"Sara Tolsma"},"openAcknowledgement":false,"status":{"submitted":true}},{"reviewer":{"displayName":"Randall DeJong"},"openAcknowledgement":false,"status":{"submitted":true}}],"curatorReviews":[]},{"id":"6b0467fd-b56c-4162-9d39-54c5477230b2","decision":"revise","abstract":"CeilingFan and Mugiwara are novel BE2 cluster siphoviruses isolated from soil samples on Streptomyces griseus ATCC 10137 and Streptomyces avermitilis NRRL 8165, respectively. CeilingFan has a genome of 132,946 bp with 49.3% G+C content, and Mugiwara has a genome of 133,330 bp with 49.1% G+C content. Both phage genomes encode 44 tRNAs and one tmRNA. The phages are assigned to the BE2 cluster of actinobacteriophages based on gene content similarity.
","acknowledgements":"
We thank members of the Howard Hughes Medical Institute Science Education Alliance-Phage Hunters Advancing Genomics and Evolutionary Science (SEA-PHAGES) program and Manuscript Data Interpretation and Nomenclature Review Team (MINT) for their support and review of the manuscript. We acknowledge Daniel French, Makayla Gomperts, and Mirkhon Normurodo at the University of Evansville who took part in the isolation of CeilingFan and University of Ottawa for isolating Mugiwara as part of their participation in the SEA-PHAGES program. We would also like to thank Dr. John Andersland (Western Kentucky University, Bowling Green, KY, USA) for providing the electron micrograph of CeilingFan.
","authors":[{"affiliations":["University of Lagos, Lagos, Nigeria"],"departments":["Department of Microbiology"],"credit":["investigation","supervision","project","validation","writing_originalDraft","writing_reviewEditing"],"email":"insa@unilag.edu.ng","firstName":"Imade Y.","lastName":"Nsa ","submittingAuthor":true,"correspondingAuthor":true,"equalContribution":false,"WBId":null,"orcid":"https://orcid.org/0000-0001-5606-268X"},{"affiliations":["University of Lagos, Lagos, Nigeria"],"departments":["Department of Microbiology"],"credit":["investigation","writing_originalDraft","writing_reviewEditing"],"email":"eziejiofor@gmail.com","firstName":"Ezichukwu E.","lastName":"Ejiofor","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":false,"WBId":null,"orcid":null},{"affiliations":["University of Lagos, Lagos, Nigeria"],"departments":["Department of Microbiology"],"credit":["investigation","writing_originalDraft","writing_reviewEditing"],"email":"ajayiemmanuel630@gmail.com","firstName":"Emmanuel T. ","lastName":"Ajayi","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":false,"WBId":null,"orcid":null},{"affiliations":["University of Lagos, Lagos, Nigeria"],"departments":["Department of Microbiology"],"credit":["investigation","writing_originalDraft","writing_reviewEditing"],"email":"okoliifunanya497@gmail.com","firstName":"Ifunanya O. ","lastName":"Okoli","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":false,"WBId":null,"orcid":null},{"affiliations":["University of Lagos, Lagos, Nigeria"],"departments":["Department of Microbiology"],"credit":["investigation","writing_originalDraft","writing_reviewEditing"],"email":"xavierchibueze@gmail.com","firstName":"Chibueze S. ","lastName":"Uchegbu","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":false,"WBId":null,"orcid":null},{"affiliations":["University of Lagos, Lagos, Nigeria"],"departments":["Department of Microbiology"],"credit":["investigation","writing_originalDraft","writing_reviewEditing"],"email":"opeoluwaaaa@gmail.com","firstName":"Opeoluwa S. ","lastName":"Aworetan","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":true,"WBId":null,"orcid":null},{"affiliations":["University of Lagos, Lagos, Nigeria"],"departments":["Department of Microbiology"],"credit":["investigation","writing_originalDraft","writing_reviewEditing"],"email":"jebfuad@gmail.com","firstName":"Fuad T.","lastName":" Jebe-Abdullah","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":true,"WBId":null,"orcid":null},{"affiliations":["University of Lagos, Lagos, Nigeria"],"departments":["Department of Microbiology"],"credit":["investigation","writing_originalDraft","writing_reviewEditing"],"email":"hauwajkam12@gmail.com","firstName":"Hauwa J.","lastName":" Kamselem","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":true,"WBId":null,"orcid":null},{"affiliations":["University of Lagos, Lagos, Nigeria"],"departments":["Department of Microbiology"],"credit":["investigation","writing_originalDraft","writing_reviewEditing"],"email":"oluwashinaabidoye@yahoo.com","firstName":"Shina O.","lastName":" Abidoye","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":true,"WBId":null,"orcid":null},{"affiliations":["University of Lagos, Lagos, Nigeria"],"departments":["Department of Microbiology"],"credit":["investigation","writing_originalDraft","writing_reviewEditing"],"email":"evansoleka6@gmail.com","firstName":"Evans C. ","lastName":"Oleka","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":true,"WBId":null,"orcid":null},{"affiliations":["University of Lagos, Lagos, Nigeria"],"departments":["Department of Microbiology"],"credit":["investigation","writing_originalDraft","writing_reviewEditing"],"email":"oluwatunkunmi@gmail.com","firstName":"Oluwatunkunmi J. ","lastName":"Okupa","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":true,"WBId":null,"orcid":null},{"affiliations":["University of Lagos, Lagos, Nigeria"],"departments":["Department of Microbiology"],"credit":["investigation","writing_originalDraft","writing_reviewEditing"],"email":"lawalfuhad51@gmail.com","firstName":"Fuhad T.","lastName":"Lawal","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":true,"WBId":null,"orcid":null},{"affiliations":["University of Lagos, Lagos, Nigeria"],"departments":["Department of Microbiology"],"credit":["investigation","writing_originalDraft","writing_reviewEditing"],"email":"immanuelgrace.o@gmail.com","firstName":"Grace O. 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","lastName":"Onyekachi","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":true,"WBId":null,"orcid":null},{"affiliations":["University of Lagos, Lagos, Nigeria"],"departments":["Department of Microbiology"],"credit":["investigation","writing_originalDraft","writing_reviewEditing"],"email":"gloriaakpederi5@gmail.com","firstName":"Omogwigho G. ","lastName":"Akpederi","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":true,"WBId":null,"orcid":null},{"affiliations":["University of Lagos, Lagos, Nigeria"],"departments":["Department of Microbiology"],"credit":["investigation","writing_originalDraft","writing_reviewEditing"],"email":"foyinsolaj@gmail.com","firstName":"Oluwafoyinsolami I. ","lastName":"Adisa","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":true,"WBId":null,"orcid":null},{"affiliations":["University of Lagos, Lagos, Nigeria"],"departments":["Department of Microbiology"],"credit":["investigation","writing_originalDraft","writing_reviewEditing"],"email":"midexy24@gmail.com","firstName":"Modesola O. ","lastName":"Onikoro","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":true,"WBId":null,"orcid":null},{"affiliations":["University of Evansville, Evansville, Indiana, United States"],"departments":["Department of Biology"],"credit":["investigation","writing_originalDraft","writing_reviewEditing"],"email":"cb508@evansville.edu","firstName":"Chase ","lastName":"Boyles","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":false,"WBId":null,"orcid":null},{"affiliations":["University of Evansville, Evansville, Indiana, United States"],"departments":["Department of Biology"],"credit":["investigation","supervision","validation","writing_originalDraft","writing_reviewEditing"],"email":"jm757@evansville.edu","firstName":"Julie A.","lastName":"Merkel","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":false,"WBId":null,"orcid":null},{"affiliations":["University of Lagos, Lagos, Nigeria"],"departments":["Department of Microbiology"],"credit":["investigation","supervision","writing_originalDraft","writing_reviewEditing"],"email":"milori@unilag.edu.ng","firstName":"Matthew O. ","lastName":"Ilori","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":false,"WBId":null,"orcid":null}],"awards":[],"conflictsOfInterest":"The authors declare that there are no conflicts of interest present.
","dataTable":{"url":"https://portal.micropublication.org/uploads/17a4a7448e5db1ccb3a096c4c5f7997a.csv"},"extendedData":[],"funding":"No funding was received to assist with the preparation of this manuscript.
","image":{"url":"https://portal.micropublication.org/uploads/855b4b16a33b0d0907ba1cd9c23ba7be.png"},"imageCaption":"(A) Plaques formed by phage Mugiwara on S. avermitilis NRRL 8165. (B) Plaques formed by phage CeilingFan on S. griseus ATCC 10137. (C) Transmission electron micrograph of Mugiwara stained with 1% uranyl acetate and imaged at 120 kV, Scale bar = 75 nm. The capsid measures 79 nm, and its tail length is 348 nm, (n=1). (D) Transmission electron micrograph (TEM) of CeilingFan stained with 1% uranyl acetate using JEOL 1400 Plus and imaged with AMT8 mixpel camera at 100 kV, Scale bar = 100 nm; the capsid diameter is [62.2 nm + 4.76, (n=10)], and the tail length is [365nm + 15.6, (n=10)].
","imageTitle":"Plaque pictures and transmission electron micrographs of CeilingFan and Mugiwara
","methods":"","reagents":"","patternDescription":"The continued discovery and characterization of Streptomyces bacteriophages improve our understanding of phage-host interactions, phage diversity, phage genome architecture, and their potential applications in combating antibiotic resistance. Streptomyces griseus subsp. griseus ATCC 10137 and Streptomyces avermitilis NRRL 8165 are bacterial type strains for studying the biology of Streptomyces (Hatfull, 2020; Kronheim et al., 2023; Rackow et al., 2024).
Here, we report the characteristics of CeilingFan and Mugiwara, isolated from slightly damp soil in Evansville, IN, USA (37.973088 N, 87.533631 W) and a grassy area near fir trees in Noertrange, Luxembourg (49.98127, 5.903158 E), respectively. Using standard protocols (Zorawik et al., 2024), CeilingFan was extracted by the enrichment method and Mugiwara by direct isolation. Briefly, soil samples were suspended in nutrient broth supplemented with glucose, MgCl2, and Ca (NO3)2, and the suspension was subsequently filtered using a 0.22 µm filter. The filtrate for Mugiwara was plated directly in top agar supplemented with S. avermitilis NRRL 8165, whereas the filtrate for CeilingFan was first inoculated with S. griseus ATCC 10137, incubated at 20 °C for 72h, and the resulting culture filtered before the filtrate was plated intop agar with S. griseus ATCC 10137. Plates for Mugiwara and CeilingFan were always incubated at 37 ˚C and 30 ˚C, with CeilingFan plates incubated for 48 hours. Mugiwara formed small, clear plaques (1.14mm +0.63, n=41), whereas CeilingFan formed slightly larger, clear plaques (1.9 mm +0.63, n=64). Both phages were purified through three rounds of plating before lysates were prepared. Transmission electron microscopy after negative staining of lysates with uranyl acetate (1%) revealed siphovirus morphology for both phages. CeilingFan has a capsid diameter of 62 nm and a tail length of 346 nm, while Mugiwara featured a larger capsid measuring 79 nm and a tail length of 348 nm (n=1) (Figure 1).
DNA was extracted from high-titer lysates of CeilingFan and Mugiwara using the Promega Wizard DNA Cleanup kit. CeilingFan and Mugiwara genomes were prepared for sequencing using the NEB Ultra II Library kit (New England Biolabs, Ipswich, MA, USA) and sequenced on the Illumina MiSeq 1000 v3 platform using the 150-bp single-end sequencing strategy at the Pittsburgh Bacteriophage Institute. Raw reads were assembled using Newbler version v3.0 (Miller et al., 2010) and checked for completeness and genomic termini using Consed v29 (Gordon et al., 1998; Russell, 2018). The number of reads generated for CeilingFan was 413,717, allowing for assembly with 466-fold coverage of a genome 132,946 bp long, with G+C content of 49.3% and a direct terminal repeat length of 12,339 bp. For Mugiwara, 342,705 reads provided 391-fold coverage of an assembled genome 133,330 bp long with G+C content of 49.1% and a direct terminal repeat length of 11,945 bp.
Auto-annotation was performed in DNA Master v 5.23.6 (http://cobamide2.bio.pitt.edu/) with Glimmer v3.02 (Delcher et al., 2007) and Genemark v2.5 (Besemer and Borodovsky, 2005), then manually refined using Starterator (http://phages.wustl.edu/starterator) for start sites comparisons (Pope and Jacobs-Sera, 2018). Functions were predicted by BLAST, using the Actinobacteriophage and NCBI non-redundant database searches v2.13.0 (Altschul et al., 1997; Russell and Hatfull, 2017), HHPRED, using the PDB_mmCIF70, (Söding, 2005), Pfam- v.36, NCBI Conserved Domains databases, Phamerator, using Actino_draft database v578 (Cresawn et al., 2011), The Observable Notebook, Subclusters (Bendele et al., 2025) and The Observable Notebook, Pham Matrices (Cobb et al., 2025). The presence of tRNAs and tmRNAs were examined using Aragorn v1.2.41 (Laslett and Canbett, 2004) and tRNAscan-SE v2.0.12 (Lowe and Eddy, 1999) and membrane proteins were identified using SOSUI v1.1 (Hirokawa et al., 1998; Mitaku & Hirokawa, 1999; Mitaku et al., 2002) and DeepTMHMM 1.0.42 (Hallgren et al., 2022). All software was used with default parameters.
Based on gene content similarity (GCS) of at least 35% to previously annotated phages within the Actinobacteriophage Database (phagesdb.org), both phages were assigned to subcluster BE2 (Russell and Hatfull, 2017; Pope et. al., 2017) and share 79% GCS with one another. CeilingFan encodes 44 predicted tRNAs, one predicted tmRNA and 248 predicted protein-coding genes, with 64 of the latter assigned putative functions; 181 genes are in the forward direction and 67 genes in the reverse direction. Mugiwara similarly encodes 44 putative tRNAs and one tmRNA and has 247 predicted protein-coding genes, of which 59 could be assigned putative functions; 183 genes are in the forward direction and 64 reverse genes.
As is typical for BE2 phages, genes encoding putative holin and endolysin proteins were identified in both CeilingFan and Mugiwara. No genes encoding a putative integrase or immunity repressor were identified in either phage, suggesting they are unlikely to establish lysogeny. MazG-like nucleotide, Ro-like RNA binding protein, DprA-like ssDNA binding protein, Cas4 exonuclease were among the functions commonly identified across BE2 phages. Mugiwara lacks the Lys-M-like peptidoglycan binding protein found in a majority of BE2 phages (23/33 phages) but it is the only BE2 member in which a putative histidine triad nucleotide binding protein has been identified. Uniquely, Mugiwara encodes a putative thioredoxin that shares little homology to the thioredoxin encoded by other BE2 phages. Similarly, CeilingFan encodes an HNH endonuclease and DNA Q-like DNA polymerase III subunit with little homology to that encoded by other BE2 phages, except for phage TomSawyer.
Nucleotide sequence accession numbers
The complete genome sequences for both phages are available at GenBank with Accession Nos. PV165877 and PV876970 and Sequence Read Archive (SRA) Nos.SRR34858420 and SRR34858425 (CeilingFan and Mugiwara respectively).
","references":[{"reference":"Altschul S. 1997. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Research 25: 3389-3402.
","pubmedId":"","doi":"10.1093/nar/25.17.3389"},{"reference":"Bendele, M., Cobb, I., and Cresawn, S. Subclusters. Accessed August 5, 2025. Observable. https://observablehq.com/d/5e5bc78c9b3ae2ed
","pubmedId":"","doi":""},{"reference":"Besemer J, Borodovsky M. 2005. GeneMark: web software for gene finding in prokaryotes, eukaryotes and viruses. Nucleic Acids Research 33: W451-W454.
","pubmedId":"","doi":"10.1093/nar/gki487"},{"reference":"Cobb, I., Cooper, K., Bendele, M., Fisher R., Jones, Z., Shifflett, Z., Cresawn, S., Pham Matrices. Accessed August 5, 2025. Observable. https://observablehq.com/@cresawn-labs/pham-matrix.
","pubmedId":"","doi":""},{"reference":"Cresawn SG, Bogel M, Day N, Jacobs-Sera D, Hendrix RW, Hatfull GF. 2011. Phamerator: a bioinformatic tool for comparative bacteriophage genomics. BMC Bioinformatics 12: 10.1186/1471-2105-12-395.
","pubmedId":"","doi":"10.1186/1471-2105-12-395"},{"reference":"Delcher AL, Bratke KA, Powers EC, Salzberg SL. 2007. Identifying bacterial genes and endosymbiont DNA with Glimmer. Bioinformatics 23: 673-679.
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","pubmedId":"","doi":"10.1101/gr.8.3.195"},{"reference":"Hallgren J, Tsirigos KD, Pedersen MD, Almagro Armenteros JJ, Marcatili P, Nielsen H, Krogh A, Winther O. 2022. DeepTMHMM predicts alpha and beta transmembrane proteins using deep neural networks. : 10.1101/2022.04.08.487609.
","pubmedId":"","doi":"10.1101/2022.04.08.487609"},{"reference":"Hatfull GF. 2020. Actinobacteriophages: Genomics, Dynamics, and Applications. Annual Review of Virology 7: 37-61.
","pubmedId":"","doi":"10.1146/annurev-virology-122019-070009"},{"reference":"Hirokawa T, Boon-Chieng S, Mitaku S. 1998. SOSUI: classification and secondary structure prediction system for membrane proteins.. Bioinformatics 14: 378-379.
","pubmedId":"","doi":"10.1093/bioinformatics/14.4.378"},{"reference":"Kronheim S, Solomon E, Ho L, Glossop M, Davidson AR, Maxwell KL. 2023. Complete genomes and comparative analyses of Streptomyces phages that influence secondary metabolism and sporulation. Scientific Reports 13: 10.1038/s41598-023-36938-z.
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","pubmedId":"","doi":"10.1016/j.ygeno.2010.03.001"},{"reference":"Mitaku S, Hirokawa T. 1999. Physicochemical factors for discriminating between soluble and membrane proteins: hydrophobicity of helical segments and protein length. Protein Engineering, Design and Selection 12: 953-957.
","pubmedId":"","doi":"10.1093/protein/12.11.953"},{"reference":"Mitaku S, Hirokawa T, Tsuji T. 2002. Amphiphilicity index of polar amino acids as an aid in the\n characterization of amino acid preference at membrane–water\n interfaces. Bioinformatics 18: 608-616.
","pubmedId":"","doi":"10.1093/bioinformatics/18.4.608"},{"reference":"Pope WH, Jacobs-Sera D. 2017. Annotation of Bacteriophage Genome Sequences Using DNA Master: An Overview. Methods in Molecular Biology,Bacteriophages : 217-229.
","pubmedId":"","doi":"10.1007/978-1-4939-7343-9_16"},{"reference":"Pope WH, Mavrich TN, Garlena RA, Guerrero-Bustamante CA, Jacobs-Sera D, Montgomery MT, et al., Hatfull. 2017. Bacteriophages of\n Gordonia\n spp. Display a Spectrum of Diversity and Genetic Relationships. mBio 8: 10.1128/mbio.01069-17.
","pubmedId":"","doi":"10.1128/mbio.01069-17"},{"reference":"Rackow B, Rolland C, Mohnen I, Wittmann J, Müsken M, Overmann Jr, Frunzke J. 2024. Isolation and characterization of the new\n Streptomyces\n phages Kamino, Geonosis, Abafar, and Scarif infecting a broad range of host species. Microbiology Spectrum 12: 10.1128/spectrum.00663-24.
","pubmedId":"","doi":"10.1128/spectrum.00663-24"},{"reference":"Russell DA. 2018. Sequencing, assembling, and finishing complete bacteriophage genomes. Methods Mol Biol 1681:109–125.
","pubmedId":"","doi":""},{"reference":"Russell DA, Hatfull GF. 2016. PhagesDB: the actinobacteriophage database. Bioinformatics 33: 784-786.
","pubmedId":"","doi":"10.1093/bioinformatics/btw711"},{"reference":"Stamm J, Merkle JA, Abernathy A, Ackerman E, Brown J, Harris A, et al., Taylor. 2024. Complete genome sequences of\n Streptomyces griseus\n phages Spelly and Phredrick. Microbiology Resource Announcements 13: 10.1128/mra.01049-23.
","pubmedId":"","doi":"10.1128/mra.01049-23"},{"reference":"Soding J, Biegert A, Lupas AN. 2005. The HHpred interactive server for protein homology detection and structure prediction. Nucleic Acids Research 33: W244-W248.
","pubmedId":"","doi":"10.1093/nar/gki408"},{"reference":"Zorawik M, Jacobs-Sera D, Freise AC, SEA-PHAGES, Reddi K. 2024. Isolation of Bacteriophages on Actinobacteria Hosts. Methods in Molecular Biology,Phage Engineering and Analysis : 273-298.
","pubmedId":"","doi":"10.1007/978-1-0716-3798-2_17 PMID: 38526736"}],"title":"Genome Sequences of Streptomyces Cluster BE2 phages CeilingFan and Mugiwara
","reviews":[{"reviewer":{"displayName":"Denise Monti"},"openAcknowledgement":false,"status":{"submitted":true}}],"curatorReviews":[]},{"id":"989f4b1e-741d-4aae-a40b-a0258492ee6d","decision":"revise","abstract":"CeilingFan and Mugiwara are novel BE2 cluster siphoviruses isolated from soil samples on Streptomyces griseus ATCC 10137 and Streptomyces avermitilis NRRL 8165, respectively. CeilingFan has a genome of 132,946 bp with 49.3% G+C content, and Mugiwara has a genome of 133,330 bp with 49.1% G+C content. Both phage genomes encode 44 tRNAs and one tmRNA. The phages are assigned to the BE2 cluster of actinobacteriophages based on gene content similarity.
","acknowledgements":"
We thank members of the Howard Hughes Medical Institute Science Education Alliance-Phage Hunters Advancing Genomics and Evolutionary Science (SEA-PHAGES) program and Manuscript Data Interpretation and Nomenclature Review Team (MINT) for their support and review of the manuscript. We acknowledge Daniel French, Makayla Gomperts, and Mirkhon Normurodo at the University of Evansville who took part in the isolation of CeilingFan and University of Ottawa for isolating Mugiwara as part of their participation in the SEA-PHAGES program. We would also like to thank Dr. John Andersland (Western Kentucky University, Bowling Green, KY, USA) for providing the electron micrograph of CeilingFan.
","authors":[{"affiliations":["University of Lagos, Lagos, Nigeria"],"departments":["Department of Microbiology"],"credit":["investigation","supervision","project","validation","writing_originalDraft","writing_reviewEditing"],"email":"insa@unilag.edu.ng","firstName":"Imade Y.","lastName":"Nsa ","submittingAuthor":true,"correspondingAuthor":true,"equalContribution":false,"WBId":null,"orcid":"https://orcid.org/0000-0001-5606-268X"},{"affiliations":["University of Lagos, Lagos, Nigeria"],"departments":["Department of Microbiology"],"credit":["investigation","writing_originalDraft","writing_reviewEditing"],"email":"eziejiofor@gmail.com","firstName":"Ezichukwu E.","lastName":"Ejiofor","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":false,"WBId":null,"orcid":null},{"affiliations":["University of Lagos, Lagos, Nigeria"],"departments":["Department of Microbiology"],"credit":["investigation","writing_originalDraft","writing_reviewEditing"],"email":"ajayiemmanuel630@gmail.com","firstName":"Emmanuel T. ","lastName":"Ajayi","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":false,"WBId":null,"orcid":null},{"affiliations":["University of Lagos, Lagos, Nigeria"],"departments":["Department of Microbiology"],"credit":["investigation","writing_originalDraft","writing_reviewEditing"],"email":"okoliifunanya497@gmail.com","firstName":"Ifunanya O. ","lastName":"Okoli","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":false,"WBId":null,"orcid":null},{"affiliations":["University of Lagos, Lagos, Nigeria"],"departments":["Department of Microbiology"],"credit":["investigation","writing_originalDraft","writing_reviewEditing"],"email":"xavierchibueze@gmail.com","firstName":"Chibueze S. ","lastName":"Uchegbu","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":false,"WBId":null,"orcid":null},{"affiliations":["University of Lagos, Lagos, Nigeria"],"departments":["Department of Microbiology"],"credit":["investigation","writing_originalDraft","writing_reviewEditing"],"email":"opeoluwaaaa@gmail.com","firstName":"Opeoluwa S. ","lastName":"Aworetan","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":true,"WBId":null,"orcid":null},{"affiliations":["University of Lagos, Lagos, Nigeria"],"departments":["Department of Microbiology"],"credit":["investigation","writing_originalDraft","writing_reviewEditing"],"email":"jebfuad@gmail.com","firstName":"Fuad T.","lastName":" Jebe-Abdullah","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":true,"WBId":null,"orcid":null},{"affiliations":["University of Lagos, Lagos, Nigeria"],"departments":["Department of Microbiology"],"credit":["investigation","writing_originalDraft","writing_reviewEditing"],"email":"hauwajkam12@gmail.com","firstName":"Hauwa J.","lastName":" Kamselem","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":true,"WBId":null,"orcid":null},{"affiliations":["University of Lagos, Lagos, Nigeria"],"departments":["Department of Microbiology"],"credit":["investigation","writing_originalDraft","writing_reviewEditing"],"email":"oluwashinaabidoye@yahoo.com","firstName":"Shina O.","lastName":" Abidoye","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":true,"WBId":null,"orcid":null},{"affiliations":["University of Lagos, Lagos, Nigeria"],"departments":["Department of Microbiology"],"credit":["investigation","writing_originalDraft","writing_reviewEditing"],"email":"evansoleka6@gmail.com","firstName":"Evans C. ","lastName":"Oleka","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":true,"WBId":null,"orcid":null},{"affiliations":["University of Lagos, Lagos, Nigeria"],"departments":["Department of Microbiology"],"credit":["investigation","writing_originalDraft","writing_reviewEditing"],"email":"oluwatunkunmi@gmail.com","firstName":"Oluwatunkunmi J. ","lastName":"Okupa","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":true,"WBId":null,"orcid":null},{"affiliations":["University of Lagos, Lagos, Nigeria"],"departments":["Department of Microbiology"],"credit":["investigation","writing_originalDraft","writing_reviewEditing"],"email":"lawalfuhad51@gmail.com","firstName":"Fuhad T.","lastName":"Lawal","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":true,"WBId":null,"orcid":null},{"affiliations":["University of Lagos, Lagos, Nigeria"],"departments":["Department of Microbiology"],"credit":["investigation","writing_originalDraft","writing_reviewEditing"],"email":"immanuelgrace.o@gmail.com","firstName":"Grace O. ","lastName":"Immanuel","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":true,"WBId":null,"orcid":null},{"affiliations":["University of Lagos, Lagos, Nigeria"],"departments":["Department of Microbiology"],"credit":["investigation","writing_originalDraft","writing_reviewEditing"],"email":"emmanueltomi3264@gmail.com","firstName":"Tomi E.","lastName":"Adeyanju","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":true,"WBId":null,"orcid":null},{"affiliations":["University of Lagos, Lagos, Nigeria"],"departments":["Department of Microbiology"],"credit":["investigation","writing_originalDraft","writing_reviewEditing"],"email":"onyekachifaith0804@gmail.com","firstName":"Faith O. ","lastName":"Onyekachi","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":true,"WBId":null,"orcid":null},{"affiliations":["University of Lagos, Lagos, Nigeria"],"departments":["Department of Microbiology"],"credit":["investigation","writing_originalDraft","writing_reviewEditing"],"email":"gloriaakpederi5@gmail.com","firstName":"Omogwigho G. ","lastName":"Akpederi","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":true,"WBId":null,"orcid":null},{"affiliations":["University of Lagos, Lagos, Nigeria"],"departments":["Department of Microbiology"],"credit":["investigation","writing_originalDraft","writing_reviewEditing"],"email":"foyinsolaj@gmail.com","firstName":"Oluwafoyinsolami I. ","lastName":"Adisa","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":true,"WBId":null,"orcid":null},{"affiliations":["University of Lagos, Lagos, Nigeria"],"departments":["Department of Microbiology"],"credit":["investigation","writing_originalDraft","writing_reviewEditing"],"email":"midexy24@gmail.com","firstName":"Modesola O. ","lastName":"Onikoro","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":true,"WBId":null,"orcid":null},{"affiliations":["University of Evansville, Evansville, Indiana, United States"],"departments":["Department of Biology"],"credit":["investigation","writing_originalDraft","writing_reviewEditing"],"email":"cb508@evansville.edu","firstName":"Chase ","lastName":"Boyles","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":false,"WBId":null,"orcid":null},{"affiliations":["University of Evansville, Evansville, Indiana, United States"],"departments":["Department of Biology"],"credit":["investigation","supervision","validation","writing_originalDraft","writing_reviewEditing"],"email":"jm757@evansville.edu","firstName":"Julie A.","lastName":"Merkel","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":false,"WBId":null,"orcid":null},{"affiliations":["University of Lagos, Lagos, Nigeria"],"departments":["Department of Microbiology"],"credit":["investigation","supervision","writing_originalDraft","writing_reviewEditing"],"email":"milori@unilag.edu.ng","firstName":"Matthew O. ","lastName":"Ilori","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":false,"WBId":null,"orcid":null}],"awards":[],"conflictsOfInterest":"The authors declare that there are no conflicts of interest present.
","dataTable":{"url":"https://portal.micropublication.org/uploads/17a4a7448e5db1ccb3a096c4c5f7997a.csv"},"extendedData":[],"funding":"No funding was received to assist with the preparation of this manuscript.
","image":{"url":"https://portal.micropublication.org/uploads/7c57b54da001dabfdfce74961adff9b2.png"},"imageCaption":"Mugiwara is on the left, and CeilingFan is on the right. Plaques formed by phage Mugiwara on S. avermitilis NRRL 8165 (top). Plaques formed by phage CeilingFan on S. griseus ATCC 10137 (top). (C) Transmission electron micrograph of Mugiwara stained with 1% uranyl acetate and imaged at 120 kV, Scale bar = 75 nm (bottom). The capsid measures 79 nm, and its tail length is 348 nm, (n=1). (D) Transmission electron micrograph (TEM) of CeilingFan stained with 1% uranyl acetate using JEOL 1400 Plus and imaged with AMT8 mixpel camera at 100 kV, Scale bar = 100 nm; the capsid diameter is [62.2 nm + 4.76, (n=10)], and the tail length is [365nm + 15.6, (n=10)] (bottom).
","imageTitle":"Plaques and Transmission Electron Micrographs of Mugiwara (left), and CeilingFan (right)
","methods":"","reagents":"","patternDescription":"The continued discovery and characterization of Streptomyces bacteriophages improve our understanding of phage-host interactions, phage diversity, phage genome architecture, and their potential applications in combating antibiotic resistance. Streptomyces griseus subsp. griseus ATCC 10137 and Streptomyces avermitilis NRRL 8165 are bacterial type strains for studying the biology of Streptomyces (Hatfull, 2020; Kronheim et al., 2023; Rackow et al., 2024).
Here, we report the characteristics of CeilingFan and Mugiwara, isolated from slightly damp soil in Evansville, IN, USA (37.973088 N, 87.533631 W) and a grassy area near fir trees in Noertrange, Luxembourg (49.98127, 5.903158 E), respectively. Using standard protocols (Zorawik et al., 2024), CeilingFan was extracted by the enrichment method and Mugiwara by direct isolation. Briefly, soil samples were suspended in nutrient broth supplemented with glucose, MgCl2, and Ca (NO3)2, and the suspension was subsequently filtered using a 0.22 µm filter. The filtrate for Mugiwara was plated directly in top agar supplemented with S. avermitilis NRRL 8165, whereas the filtrate for CeilingFan was first inoculated with S. griseus ATCC 10137, incubated at 20 °C for 72h, and the resulting culture filtered before the filtrate was plated intop agar with S. griseus ATCC 10137. Plates for Mugiwara and CeilingFan were always incubated at 37 ˚C and 30 ˚C, with CeilingFan plates incubated for 48 hours. Mugiwara formed small, clear plaques (1.14 mm +0.63, n=41 (Schnieder et al., 2012)), whereas CeilingFan formed slightly larger, clear plaques (1.9 mm +0.63, n=64 (Cacciabue et al., 2019)). Both phages were purified through three rounds of plating before lysates were prepared. Transmission electron microscopy after negative staining of lysates with uranyl acetate (1%) revealed siphovirus morphology for both phages. CeilingFan has a capsid diameter of 62 nm and a tail length of 346 nm, while Mugiwara featured a larger capsid measuring 79 nm and a tail length of 348 nm (n=1) (Figure 1).
DNA was extracted from high-titer lysates of CeilingFan and Mugiwara using the Promega Wizard DNA Cleanup kit. CeilingFan and Mugiwara genomes were prepared for sequencing using the NEB Ultra II Library kit (New England Biolabs, Ipswich, MA, USA) and sequenced on the Illumina MiSeq 1000 v3 platform using the 150-bp single-end sequencing strategy at the Pittsburgh Bacteriophage Institute. Raw reads were assembled using Newbler version v3.0 (Miller et al., 2010) and checked for completeness and genomic termini using Consed v29 (Gordon et al., 1998; Russell, 2018). The number of reads generated for CeilingFan was 413,717, allowing for assembly with 466-fold coverage of a genome 132,946 bp long, with G+C content of 49.3% and a direct terminal repeat length of 12,339 bp. For Mugiwara, 342,705 reads provided 391-fold coverage of an assembled genome 133,330 bp long with G+C content of 49.1% and a direct terminal repeat length of 11,945 bp.
Auto-annotation was performed in DNA Master v 5.23.6 (http://cobamide2.bio.pitt.edu/) with Glimmer v3.02 (Delcher et al., 2007) and Genemark v2.5 (Besemer and Borodovsky, 2005), then manually refined using Starterator (http://phages.wustl.edu/starterator) for start sites comparisons (Pope and Jacobs-Sera, 2018). Functions were predicted by BLAST, using the Actinobacteriophage and NCBI non-redundant database searches v2.13.0 (Altschul et al., 1997; Russell and Hatfull, 2017), HHPRED, using the PDB_mmCIF70, (Söding, 2005), Pfam- v.36, NCBI Conserved Domains databases, Phamerator, using Actino_draft database v578 (Cresawn et al., 2011), The Observable Notebook, Subclusters (Bendele et al., 2025) and The Observable Notebook, Pham Matrices (Cobb et al., 2025). The presence of tRNAs and tmRNAs were examined using Aragorn v1.2.41 (Laslett and Canbett, 2004) and tRNAscan-SE v2.0.12 (Lowe and Eddy, 1999) and membrane proteins were identified using SOSUI v1.1 (Hirokawa et al., 1998; Mitaku & Hirokawa, 1999; Mitaku et al., 2002) and DeepTMHMM 1.0.42 (Hallgren et al., 2022). All software was used with default parameters.
Based on gene content similarity (GCS) of at least 35% to previously annotated phages within the Actinobacteriophage Database (phagesdb.org), both phages were assigned to subcluster BE2 (Russell and Hatfull, 2017; Pope et. al., 2017) and share 79% GCS with one another. CeilingFan encodes 44 predicted tRNAs, one predicted tmRNA and 248 predicted protein-coding genes, with 64 of the latter assigned putative functions; 181 genes are in the forward direction and 67 genes in the reverse direction. Mugiwara similarly encodes 44 putative tRNAs and one tmRNA and has 247 predicted protein-coding genes, of which 59 could be assigned putative functions; 183 genes are in the forward direction and 64 reverse genes.
As is typical for BE2 phages, genes encoding putative holin and endolysin proteins were identified in both CeilingFan and Mugiwara. No genes encoding a putative integrase or immunity repressor were identified in either phage, suggesting they are unlikely to establish lysogeny. MazG-like nucleotide, Ro-like RNA binding protein, DprA-like ssDNA binding protein, Cas4 exonuclease were among the functions commonly identified across BE2 phages. Mugiwara lacks the Lys-M-like peptidoglycan binding protein found in a majority of BE2 phages (23/33 phages) but it is the only BE2 member in which a putative histidine triad nucleotide binding protein has been identified. Uniquely, Mugiwara encodes a putative thioredoxin that shares little homology to the thioredoxin encoded by other BE2 phages. Similarly, CeilingFan encodes an HNH endonuclease and DNA Q-like DNA polymerase III subunit with little homology to that encoded by other BE2 phages, except for phage TomSawyer.
Nucleotide sequence accession numbers
The complete genome sequences for both phages are available at GenBank with Accession Nos. PV165877 and PV876970 and Sequence Read Archive (SRA) Nos.SRR34858420 and SRR34858425 (CeilingFan and Mugiwara respectively).
","references":[{"reference":"Altschul S. 1997. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Research 25: 3389-3402.
","pubmedId":"","doi":"10.1093/nar/25.17.3389"},{"reference":"Bendele M, Cobb I, and Cresawn S. Subclusters. Accessed August 5, 2025. Observable. https://observablehq.com/d/5e5bc78c9b3ae2ed
","pubmedId":"","doi":""},{"reference":"Besemer J, Borodovsky M. 2005. GeneMark: web software for gene finding in prokaryotes, eukaryotes and viruses. Nucleic Acids Research 33: W451-W454.
","pubmedId":"","doi":"10.1093/nar/gki487"},{"reference":"Cacciabue M, Currá A, Gismondi MI. 2019. ViralPlaque: a Fiji macro for automated assessment of viral plaque statistics. PeerJ 7: e7729.
","pubmedId":"","doi":"10.7717/peerj.7729"},{"reference":"Cobb I, Cooper K, Bendele M, Fisher R, Jones, Z, Shifflett Z, Cresawn S. Pham Matrices. Accessed August 5, 2025. Observable. https://observablehq.com/@cresawn-labs/pham-matrix.
","pubmedId":"","doi":""},{"reference":"Cresawn SG, Bogel M, Day N, Jacobs-Sera D, Hendrix RW, Hatfull GF. 2011. Phamerator: a bioinformatic tool for comparative bacteriophage genomics. BMC Bioinformatics 12: 10.1186/1471-2105-12-395.
","pubmedId":"","doi":"10.1186/1471-2105-12-395"},{"reference":"Delcher AL, Bratke KA, Powers EC, Salzberg SL. 2007. Identifying bacterial genes and endosymbiont DNA with Glimmer. Bioinformatics 23: 673-679.
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","pubmedId":"","doi":"10.1093/protein/12.11.953"},{"reference":"Mitaku S, Hirokawa T, Tsuji T. 2002. Amphiphilicity index of polar amino acids as an aid in the\n characterization of amino acid preference at membrane–water\n interfaces. Bioinformatics 18: 608-616.
","pubmedId":"","doi":"10.1093/bioinformatics/18.4.608"},{"reference":"Pope WH, Jacobs-Sera D. 2017. Annotation of Bacteriophage Genome Sequences Using DNA Master: An Overview. Methods in Molecular Biology,Bacteriophages : 217-229.
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","pubmedId":"","doi":"10.1038nmeth.2089"},{"reference":"Stamm J, Merkle JA, Abernathy A, Ackerman E, Brown J, Harris A, Hoffman K, Hoskins A, Jahn A, Jones N, Kitch A, Mathavan N, Rose N, Taylor J. 2024.Complete genome sequences of Streptomyces griseus phages Spelly and Phredrick. Microbiol Resour Announc13:e01049-23.https://doi.org/10.1128/mra.01049-23
","pubmedId":"","doi":"10.1128/mra.01049-23"},{"reference":"Soding J, Biegert A, Lupas AN. 2005. The HHpred interactive server for protein homology detection and structure prediction. Nucleic Acids Research 33: W244-W248.
","pubmedId":"","doi":"10.1093/nar/gki408"},{"reference":"Zorawik M, Jacobs-Sera D, Freise AC, SEA-PHAGES, Reddi K. 2024. Isolation of Bacteriophages on Actinobacteria Hosts. Methods in Molecular Biology,Phage Engineering and Analysis : 273-298.
","pubmedId":"","doi":"10.1007/978-1-0716-3798-2_17 PMID: 38526736"}],"title":"Genome Sequences of Streptomyces Cluster BE2 phages CeilingFan and Mugiwara
","reviews":[],"curatorReviews":[]},{"id":"d698b9ba-8674-4384-be96-7317627d9590","decision":"edit","abstract":"CeilingFan and Mugiwara are novel BE2 cluster siphoviruses isolated from soil samples on Streptomyces griseus ATCC 10137 and Streptomyces avermitilis NRRL 8165, respectively. CeilingFan has a genome of 132,946 bp with 49.3% G+C content, and Mugiwara has a genome of 133,330 bp with 49.1% G+C content. Both phage genomes encode 44 tRNAs and one tmRNA. The phages are assigned to the BE2 cluster of actinobacteriophages based on gene content similarity.
","acknowledgements":"
We thank members of the Howard Hughes Medical Institute Science Education Alliance-Phage Hunters Advancing Genomics and Evolutionary Science (SEA-PHAGES) program and Manuscript Data Interpretation and Nomenclature Review Team (MINT) for their support and review of the manuscript. We acknowledge Daniel French, Makayla Gomperts, and Mirkhon Normurodo at the University of Evansville who took part in the isolation of CeilingFan and University of Ottawa for isolating Mugiwara as part of their participation in the SEA-PHAGES program. We would also like to thank Dr. John Andersland (Western Kentucky University, Bowling Green, KY, USA) for providing the electron micrograph of CeilingFan.
","authors":[{"affiliations":["University of Lagos, Lagos, Nigeria"],"departments":["Department of Microbiology"],"credit":["investigation","supervision","project","validation","writing_originalDraft","writing_reviewEditing"],"email":"insa@unilag.edu.ng","firstName":"Imade Y.","lastName":"Nsa ","submittingAuthor":true,"correspondingAuthor":true,"equalContribution":false,"WBId":null,"orcid":"https://orcid.org/0000-0001-5606-268X"},{"affiliations":["University of Lagos, Lagos, Nigeria"],"departments":["Department of Microbiology"],"credit":["investigation","writing_originalDraft","writing_reviewEditing"],"email":"eziejiofor@gmail.com","firstName":"Ezichukwu E.","lastName":"Ejiofor","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":false,"WBId":null,"orcid":null},{"affiliations":["University of Lagos, Lagos, Nigeria"],"departments":["Department of Microbiology"],"credit":["investigation","writing_originalDraft","writing_reviewEditing"],"email":"ajayiemmanuel630@gmail.com","firstName":"Emmanuel T. ","lastName":"Ajayi","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":false,"WBId":null,"orcid":null},{"affiliations":["University of Lagos, Lagos, Nigeria"],"departments":["Department of Microbiology"],"credit":["investigation","writing_originalDraft","writing_reviewEditing"],"email":"okoliifunanya497@gmail.com","firstName":"Ifunanya O. ","lastName":"Okoli","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":false,"WBId":null,"orcid":null},{"affiliations":["University of Lagos, Lagos, Nigeria"],"departments":["Department of Microbiology"],"credit":["investigation","writing_originalDraft","writing_reviewEditing"],"email":"xavierchibueze@gmail.com","firstName":"Chibueze S. ","lastName":"Uchegbu","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":false,"WBId":null,"orcid":null},{"affiliations":["University of Lagos, Lagos, Nigeria"],"departments":["Department of Microbiology"],"credit":["investigation","writing_originalDraft","writing_reviewEditing"],"email":"opeoluwaaaa@gmail.com","firstName":"Opeoluwa S. ","lastName":"Aworetan","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":true,"WBId":null,"orcid":null},{"affiliations":["University of Lagos, Lagos, Nigeria"],"departments":["Department of Microbiology"],"credit":["investigation","writing_originalDraft","writing_reviewEditing"],"email":"jebfuad@gmail.com","firstName":"Fuad T.","lastName":" Jebe-Abdullah","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":true,"WBId":null,"orcid":null},{"affiliations":["University of Lagos, Lagos, Nigeria"],"departments":["Department of Microbiology"],"credit":["investigation","writing_originalDraft","writing_reviewEditing"],"email":"hauwajkam12@gmail.com","firstName":"Hauwa J.","lastName":" Kamselem","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":true,"WBId":null,"orcid":null},{"affiliations":["University of Lagos, Lagos, Nigeria"],"departments":["Department of Microbiology"],"credit":["investigation","writing_originalDraft","writing_reviewEditing"],"email":"oluwashinaabidoye@yahoo.com","firstName":"Shina O.","lastName":" Abidoye","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":true,"WBId":null,"orcid":null},{"affiliations":["University of Lagos, Lagos, Nigeria"],"departments":["Department of Microbiology"],"credit":["investigation","writing_originalDraft","writing_reviewEditing"],"email":"evansoleka6@gmail.com","firstName":"Evans C. ","lastName":"Oleka","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":true,"WBId":null,"orcid":null},{"affiliations":["University of Lagos, Lagos, Nigeria"],"departments":["Department of Microbiology"],"credit":["investigation","writing_originalDraft","writing_reviewEditing"],"email":"oluwatunkunmi@gmail.com","firstName":"Oluwatunkunmi J. ","lastName":"Okupa","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":true,"WBId":null,"orcid":null},{"affiliations":["University of Lagos, Lagos, Nigeria"],"departments":["Department of Microbiology"],"credit":["investigation","writing_originalDraft","writing_reviewEditing"],"email":"lawalfuhad51@gmail.com","firstName":"Fuhad T.","lastName":"Lawal","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":true,"WBId":null,"orcid":null},{"affiliations":["University of Lagos, Lagos, Nigeria"],"departments":["Department of Microbiology"],"credit":["investigation","writing_originalDraft","writing_reviewEditing"],"email":"immanuelgrace.o@gmail.com","firstName":"Grace O. ","lastName":"Immanuel","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":true,"WBId":null,"orcid":null},{"affiliations":["University of Lagos, Lagos, Nigeria"],"departments":["Department of Microbiology"],"credit":["investigation","writing_originalDraft","writing_reviewEditing"],"email":"emmanueltomi3264@gmail.com","firstName":"Tomi E.","lastName":"Adeyanju","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":true,"WBId":null,"orcid":null},{"affiliations":["University of Lagos, Lagos, Nigeria"],"departments":["Department of Microbiology"],"credit":["investigation","writing_originalDraft","writing_reviewEditing"],"email":"onyekachifaith0804@gmail.com","firstName":"Faith O. ","lastName":"Onyekachi","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":true,"WBId":null,"orcid":null},{"affiliations":["University of Lagos, Lagos, Nigeria"],"departments":["Department of Microbiology"],"credit":["investigation","writing_originalDraft","writing_reviewEditing"],"email":"gloriaakpederi5@gmail.com","firstName":"Omogwigho G. ","lastName":"Akpederi","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":true,"WBId":null,"orcid":null},{"affiliations":["University of Lagos, Lagos, Nigeria"],"departments":["Department of Microbiology"],"credit":["investigation","writing_originalDraft","writing_reviewEditing"],"email":"foyinsolaj@gmail.com","firstName":"Oluwafoyinsolami I. ","lastName":"Adisa","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":true,"WBId":null,"orcid":null},{"affiliations":["University of Lagos, Lagos, Nigeria"],"departments":["Department of Microbiology"],"credit":["investigation","writing_originalDraft","writing_reviewEditing"],"email":"midexy24@gmail.com","firstName":"Modesola O. ","lastName":"Onikoro","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":true,"WBId":null,"orcid":null},{"affiliations":["University of Evansville, Evansville, Indiana, United States"],"departments":["Department of Biology"],"credit":["investigation","writing_originalDraft","writing_reviewEditing"],"email":"cb508@evansville.edu","firstName":"Chase ","lastName":"Boyles","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":false,"WBId":null,"orcid":null},{"affiliations":["University of Evansville, Evansville, Indiana, United States"],"departments":["Department of Biology"],"credit":["investigation","supervision","validation","writing_originalDraft","writing_reviewEditing"],"email":"jm757@evansville.edu","firstName":"Julie A.","lastName":"Merkel","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":false,"WBId":null,"orcid":null},{"affiliations":["University of Lagos, Lagos, Nigeria"],"departments":["Department of Microbiology"],"credit":["investigation","supervision","writing_originalDraft","writing_reviewEditing"],"email":"milori@unilag.edu.ng","firstName":"Matthew O. ","lastName":"Ilori","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":false,"WBId":null,"orcid":null}],"awards":[],"conflictsOfInterest":"The authors declare that there are no conflicts of interest present.
","dataTable":{"url":"https://portal.micropublication.org/uploads/17a4a7448e5db1ccb3a096c4c5f7997a.csv"},"extendedData":[],"funding":"No funding was received to assist with the preparation of this manuscript.
","image":{"url":"https://portal.micropublication.org/uploads/e47df77b39a4d878d38641c884e58a9d.png"},"imageCaption":"Mugiwara is on the left, and CeilingFan is on the right. Plaques formed by phage Mugiwara on S. avermitilis NRRL 8165 (top). Plaques formed by phage CeilingFan on S. griseus ATCC 10137 (top). (C) Transmission electron micrograph of Mugiwara stained with 1% uranyl acetate and imaged at 120 kV, Scale bar = 75 nm (bottom). The capsid measures 79 nm, and its tail length is 348 nm, (n=1). (D) Transmission electron micrograph (TEM) of CeilingFan stained with 1% uranyl acetate using JEOL 1400 Plus and imaged with AMT8 mixpel camera at 100 kV, Scale bar = 100 nm; the capsid diameter is [62.2 nm + 4.76, (n=10)], and the tail length is [365nm + 15.6, (n=10)] (bottom).
","imageTitle":"Plaques and Transmission Electron Micrographs of Mugiwara (left), and CeilingFan (right)
","methods":"","reagents":"","patternDescription":"The continued discovery and characterization of Streptomyces bacteriophages improve our understanding of phage-host interactions, phage diversity, phage genome architecture, and their potential applications in combating antibiotic resistance. Streptomyces griseus subsp. griseus ATCC 10137 and Streptomyces avermitilis NRRL 8165 are bacterial type strains for studying the biology of Streptomyces (Hatfull, 2020; Kronheim et al., 2023; Rackow et al., 2024).
Here, we report the characteristics of CeilingFan and Mugiwara, isolated from slightly damp soil in Evansville, IN, USA (37.973088 N, 87.533631 W) and a grassy area near fir trees in Noertrange, Luxembourg (49.98127, 5.903158 E), respectively. Using standard protocols (Zorawik et al., 2024), CeilingFan was extracted by the enrichment method and Mugiwara by direct isolation. Briefly, soil samples were suspended in nutrient broth supplemented with glucose, MgCl2, and Ca (NO3)2, and the suspension was subsequently filtered using a 0.22 µm filter. The filtrate for Mugiwara was plated directly in top agar supplemented with S. avermitilis NRRL 8165, whereas the filtrate for CeilingFan was first inoculated with S. griseus ATCC 10137, incubated at 20 °C for 72h, and the resulting culture filtered before the filtrate was plated in top agar with S. griseus ATCC 10137. Plates for Mugiwara and CeilingFan were always incubated at 37 ˚C and 30 ˚C, with CeilingFan plates incubated for 48 hours. Mugiwara formed small, clear plaques (1.14 mm +0.63, n=41 (Schnieder et al., 2012)), whereas CeilingFan formed slightly larger, clear plaques (1.9 mm +0.63, n=64 (Cacciabue et al., 2019)). Both phages were purified through three rounds of plating before lysates were prepared. Transmission electron microscopy after negative staining of lysates with uranyl acetate (1%) revealed siphovirus morphology for both phages. CeilingFan has a capsid diameter of 62 nm and a tail length of 346 nm, while Mugiwara featured a larger capsid measuring 79 nm and a tail length of 348 nm (n=1) (Figure 1).
DNA was extracted from high-titer lysates of CeilingFan and Mugiwara using the Promega Wizard DNA Cleanup kit. CeilingFan and Mugiwara genomes were prepared for sequencing using the NEB Ultra II Library kit (New England Biolabs, Ipswich, MA, USA) and sequenced on the Illumina MiSeq 1000 v3 platform using the 150-bp single-end sequencing strategy at the Pittsburgh Bacteriophage Institute. Raw reads were assembled using Newbler version v3.0 (Miller et al., 2010) and checked for completeness and genomic termini using Consed v29 (Gordon et al., 1998; Russell, 2018). The number of reads generated for CeilingFan was 413,717, allowing for assembly with 466-fold coverage of a genome 132,946 bp long, with G+C content of 49.3% and a direct terminal repeat length of 12,339 bp. For Mugiwara, 342,705 reads provided 391-fold coverage of an assembled genome 133,330 bp long with G+C content of 49.1% and a direct terminal repeat length of 11,945 bp.
Auto-annotation was performed in DNA Master v 5.23.6 (http://cobamide2.bio.pitt.edu/) with Glimmer v3.02 (Delcher et al., 2007) and Genemark v2.5 (Besemer and Borodovsky, 2005), then manually refined using Starterator (http://phages.wustl.edu/starterator) for start sites comparisons (Pope and Jacobs-Sera, 2018). Functions were predicted by BLAST, using the Actinobacteriophage and NCBI non-redundant database searches v2.13.0 (Altschul et al., 1997; Russell and Hatfull, 2017), HHPRED, using the PDB_mmCIF70, (Söding, 2005), Pfam- v.36, NCBI Conserved Domains databases, Phamerator, using Actino_draft database v578 (Cresawn et al., 2011), The Observable Notebook, Subclusters (Bendele et al., 2025) and The Observable Notebook, Pham Matrices (Cobb et al., 2025). The presence of tRNAs and tmRNAs were examined using Aragorn v1.2.41 (Laslett and Canbett, 2004) and tRNAscan-SE v2.0.12 (Lowe and Eddy, 1999) and membrane proteins were identified using SOSUI v1.1 (Hirokawa et al., 1998; Mitaku & Hirokawa, 1999; Mitaku et al., 2002) and DeepTMHMM 1.0.42 (Hallgren et al., 2022). All software was used with default parameters.
Based on gene content similarity (GCS) of at least 35% to previously annotated phages within the Actinobacteriophage Database (phagesdb.org), both phages were assigned to subcluster BE2 (Russell and Hatfull, 2017; Pope et. al., 2017) and share 79% GCS with one another. CeilingFan encodes 44 predicted tRNAs, one predicted tmRNA and 248 predicted protein-coding genes, with 64 of the latter assigned putative functions; 181 genes are in the forward direction and 67 genes in the reverse direction. Mugiwara similarly encodes 44 putative tRNAs and one tmRNA and has 247 predicted protein-coding genes, of which 59 could be assigned putative functions; 183 genes are in the forward direction and 64 reverse genes.
As is typical for BE2 phages, genes encoding putative holin and endolysin proteins were identified in both CeilingFan and Mugiwara. No genes encoding a putative integrase or immunity repressor were identified in either phage, suggesting they are unlikely to establish lysogeny. MazG-like nucleotide, Ro-like RNA binding protein, DprA-like ssDNA binding protein, Cas4 exonuclease were among the functions commonly identified across BE2 phages. Mugiwara lacks the Lys-M-like peptidoglycan binding protein found in a majority of BE2 phages (23/33 phages) but it is the only BE2 member in which a putative histidine triad nucleotide binding protein has been identified. Uniquely, Mugiwara encodes a putative thioredoxin that shares little homology to the thioredoxin encoded by other BE2 phages. Similarly, CeilingFan encodes an HNH endonuclease and DNA Q-like DNA polymerase III subunit with little homology to that encoded by other BE2 phages, except for phage TomSawyer.
Nucleotide sequence accession numbers
The complete genome sequences for both phages are available at GenBank with Accession Nos. PV165877 and PV876970 and Sequence Read Archive (SRA) Nos.SRR34858420 and SRR34858425 (CeilingFan and Mugiwara respectively).
","references":[{"reference":"Altschul S. 1997. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Research 25: 3389-3402.
","pubmedId":"","doi":"10.1093/nar/25.17.3389"},{"reference":"Bendele M, Cobb I, and Cresawn S. Subclusters. Accessed August 5, 2025. Observable. https://observablehq.com/d/5e5bc78c9b3ae2ed
","pubmedId":"","doi":""},{"reference":"Besemer J, Borodovsky M. 2005. GeneMark: web software for gene finding in prokaryotes, eukaryotes and viruses. Nucleic Acids Research 33: W451-W454.
","pubmedId":"","doi":"10.1093/nar/gki487"},{"reference":"Cacciabue M, Currá A, Gismondi MI. 2019. ViralPlaque: a Fiji macro for automated assessment of viral plaque statistics. PeerJ 7: e7729.
","pubmedId":"","doi":"10.7717/peerj.7729"},{"reference":"Cobb I, Cooper K, Bendele M, Fisher R, Jones, Z, Shifflett Z, Cresawn S. Pham Matrices. Accessed August 5, 2025. Observable. https://observablehq.com/@cresawn-labs/pham-matrix.
","pubmedId":"","doi":""},{"reference":"Cresawn SG, Bogel M, Day N, Jacobs-Sera D, Hendrix RW, Hatfull GF. 2011. Phamerator: a bioinformatic tool for comparative bacteriophage genomics. BMC Bioinformatics 12: 10.1186/1471-2105-12-395.
","pubmedId":"","doi":"10.1186/1471-2105-12-395"},{"reference":"Delcher AL, Bratke KA, Powers EC, Salzberg SL. 2007. Identifying bacterial genes and endosymbiont DNA with Glimmer. Bioinformatics 23: 673-679.
","pubmedId":"","doi":"10.1093/bioinformatics/btm009"},{"reference":"Gordon D, Abajian C, Green P. 1998. Consed: A Graphical Tool for Sequence Finishing. Genome Research 8: 195-202.
","pubmedId":"","doi":"10.1101/gr.8.3.195"},{"reference":"Hallgren J, Tsirigos KD, Pedersen MD, Almagro Armenteros JJ, Marcatili P, Nielsen H, Krogh A, Winther O. 2022. DeepTMHMM predicts alpha and beta transmembrane proteins using deep neural networks. : 10.1101/2022.04.08.487609.
","pubmedId":"","doi":"10.1101/2022.04.08.487609"},{"reference":"Hatfull GF. 2020. Actinobacteriophages: Genomics, Dynamics, and Applications. Annual Review of Virology 7: 37-61.
","pubmedId":"","doi":"10.1146/annurev-virology-122019-070009"},{"reference":"Hirokawa T, Boon-Chieng S, Mitaku S. 1998. SOSUI: classification and secondary structure prediction system for membrane proteins.. Bioinformatics 14: 378-379.
","pubmedId":"","doi":"10.1093/bioinformatics/14.4.378"},{"reference":"Kronheim S, Solomon E, Ho L, Glossop M, Davidson AR, Maxwell KL. 2023. Complete genomes and comparative analyses of Streptomyces phages that influence secondary metabolism and sporulation. Scientific Reports 13: 10.1038/s41598-023-36938-z.
","pubmedId":"","doi":"10.1038/s41598-023-36938-z"},{"reference":"Laslett D. 2004. ARAGORN, a program to detect tRNA genes and tmRNA genes in nucleotide sequences. Nucleic Acids Research 32: 11-16.
","pubmedId":"","doi":"10.1093/nar/gkh152"},{"reference":"Lowe TM, Eddy SR. 1997. tRNAscan-SE: A Program for Improved Detection of Transfer RNA Genes in Genomic Sequence. Nucleic Acids Research 25: 955-964.
","pubmedId":"","doi":"10.1093/nar/25.5.955 "},{"reference":"Miller JR, Koren S, Sutton G. 2010. Assembly algorithms for next-generation sequencing data. Genomics 95: 315-327.
","pubmedId":"","doi":"10.1016/j.ygeno.2010.03.001"},{"reference":"Mitaku S, Hirokawa T. 1999. Physicochemical factors for discriminating between soluble and membrane proteins: hydrophobicity of helical segments and protein length. Protein Engineering, Design and Selection 12: 953-957.
","pubmedId":"","doi":"10.1093/protein/12.11.953"},{"reference":"Mitaku S, Hirokawa T, Tsuji T. 2002. Amphiphilicity index of polar amino acids as an aid in the\n characterization of amino acid preference at membrane–water\n interfaces. Bioinformatics 18: 608-616.
","pubmedId":"","doi":"10.1093/bioinformatics/18.4.608"},{"reference":"Pope WH, Jacobs-Sera D. 2017. Annotation of Bacteriophage Genome Sequences Using DNA Master: An Overview. Methods in Molecular Biology,Bacteriophages : 217-229.
","pubmedId":"","doi":"10.1007/978-1-4939-7343-9_16"},{"reference":"Pope WH, Mavrich TN, Garlena RA, Guerrero-Bustamante CA, Jacobs-Sera D, Montgomery MT, et al., Hatfull GF. 2017. Bacteriophages of Gordonia spp. Display a Spectrum of Diversity and Genetic Relationships. mBio 8: 10.1128/mbio.01069-17.
","pubmedId":"","doi":"10.1128/mbio.01069-17"},{"reference":"Rackow B, Rolland C, Mohnen I, Wittmann J, Müsken M, Overmann Jr, Frunzke J. 2024. Isolation and characterization of the new\n Streptomyces\n phages Kamino, Geonosis, Abafar, and Scarif infecting a broad range of host species. Microbiology Spectrum 12: 10.1128/spectrum.00663-24.
","pubmedId":"","doi":"10.1128/spectrum.00663-24"},{"reference":"Russell DA. 2018. Sequencing, assembling, and finishing complete bacteriophage genomes. Methods Mol Biol 1681:109–125.
","pubmedId":"","doi":""},{"reference":"Russell DA, Hatfull GF. 2016. PhagesDB: the actinobacteriophage database. Bioinformatics 33: 784-786.
","pubmedId":"","doi":"10.1093/bioinformatics/btw711"},{"reference":"Schneider, CA, Rasband, WS, & Eliceiri, KW. (2012). NIH Image to ImageJ: 25 years of image analysis. Nature Methods, 9(7), 671–675
","pubmedId":"","doi":"10.1038nmeth.2089"},{"reference":"Stamm J, Merkle JA, Abernathy A, Ackerman E, Brown J, Harris A, Hoffman K, Hoskins A, Jahn A, Jones N, Kitch A, Mathavan N, Rose N, Taylor J. 2024.Complete genome sequences of Streptomyces griseus phages Spelly and Phredrick. Microbiol Resour Announc13:e01049-23.https://doi.org/10.1128/mra.01049-23
","pubmedId":"","doi":"10.1128/mra.01049-23"},{"reference":"Soding J, Biegert A, Lupas AN. 2005. The HHpred interactive server for protein homology detection and structure prediction. Nucleic Acids Research 33: W244-W248.
","pubmedId":"","doi":"10.1093/nar/gki408"},{"reference":"Zorawik M, Jacobs-Sera D, Freise AC, SEA-PHAGES, Reddi K. 2024. Isolation of Bacteriophages on Actinobacteria Hosts. Methods in Molecular Biology,Phage Engineering and Analysis : 273-298.
","pubmedId":"","doi":"10.1007/978-1-0716-3798-2_17 PMID: 38526736"}],"title":"Genome Sequences of Streptomyces Cluster BE2 phages CeilingFan and Mugiwara
","reviews":[],"curatorReviews":[]},{"id":"99ed16f4-c064-4d2c-a97d-f394084dc476","decision":"accept","abstract":"CeilingFan and Mugiwara are novel BE2 cluster siphoviruses isolated from soil samples on Streptomyces griseus ATCC 10137 and Streptomyces avermitilis NRRL 8165, respectively. CeilingFan has a genome of 132,946 bp with 49.3% G+C content, and Mugiwara has a genome of 133,330 bp with 49.1% G+C content. Both phage genomes encode 44 tRNAs and one tmRNA. The phages are assigned to the BE2 cluster of actinobacteriophages based on gene content similarity.
","acknowledgements":"We thank members of the Howard Hughes Medical Institute Science Education Alliance-Phage Hunters Advancing Genomics and Evolutionary Science (SEA-PHAGES) program and Manuscript Data Interpretation and Nomenclature Review Team (MINT) for their support and review of the manuscript. We acknowledge Daniel French, Makayla Gomperts, and Mirkhon Normurodo at the University of Evansville who took part in the isolation of CeilingFan and University of Ottawa for isolating Mugiwara as part of their participation in the SEA-PHAGES program. We would also like to thank Dr. John Andersland (Western Kentucky University, Bowling Green, KY, USA) for providing the electron micrograph of CeilingFan.
","authors":[{"affiliations":["University of Lagos, Lagos, Nigeria"],"departments":["Department of Microbiology"],"credit":["investigation","supervision","project","validation","writing_originalDraft","writing_reviewEditing"],"email":"insa@unilag.edu.ng","firstName":"Imade Y.","lastName":"Nsa ","submittingAuthor":true,"correspondingAuthor":true,"equalContribution":false,"WBId":null,"orcid":"https://orcid.org/0000-0001-5606-268X"},{"affiliations":["University of Lagos, Lagos, Nigeria"],"departments":["Department of Microbiology"],"credit":["investigation","writing_originalDraft","writing_reviewEditing"],"email":"eziejiofor@gmail.com","firstName":"Ezichukwu E.","lastName":"Ejiofor","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":false,"WBId":null,"orcid":null},{"affiliations":["University of Lagos, Lagos, Nigeria"],"departments":["Department of Microbiology"],"credit":["investigation","writing_originalDraft","writing_reviewEditing"],"email":"ajayiemmanuel630@gmail.com","firstName":"Emmanuel T. ","lastName":"Ajayi","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":false,"WBId":null,"orcid":null},{"affiliations":["University of Lagos, Lagos, Nigeria"],"departments":["Department of Microbiology"],"credit":["investigation","writing_originalDraft","writing_reviewEditing"],"email":"okoliifunanya497@gmail.com","firstName":"Ifunanya O. ","lastName":"Okoli","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":false,"WBId":null,"orcid":null},{"affiliations":["University of Lagos, Lagos, Nigeria"],"departments":["Department of Microbiology"],"credit":["investigation","writing_originalDraft","writing_reviewEditing"],"email":"xavierchibueze@gmail.com","firstName":"Chibueze S. ","lastName":"Uchegbu","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":false,"WBId":null,"orcid":null},{"affiliations":["University of Lagos, Lagos, Nigeria"],"departments":["Department of Microbiology"],"credit":["investigation","writing_originalDraft","writing_reviewEditing"],"email":"opeoluwaaaa@gmail.com","firstName":"Opeoluwa S. ","lastName":"Aworetan","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":true,"WBId":null,"orcid":null},{"affiliations":["University of Lagos, Lagos, Nigeria"],"departments":["Department of Microbiology"],"credit":["investigation","writing_originalDraft","writing_reviewEditing"],"email":"jebfuad@gmail.com","firstName":"Fuad T.","lastName":" Jebe-Abdullah","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":true,"WBId":null,"orcid":null},{"affiliations":["University of Lagos, Lagos, Nigeria"],"departments":["Department of Microbiology"],"credit":["investigation","writing_originalDraft","writing_reviewEditing"],"email":"hauwajkam12@gmail.com","firstName":"Hauwa J.","lastName":" Kamselem","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":true,"WBId":null,"orcid":null},{"affiliations":["University of Lagos, Lagos, Nigeria"],"departments":["Department of Microbiology"],"credit":["investigation","writing_originalDraft","writing_reviewEditing"],"email":"oluwashinaabidoye@yahoo.com","firstName":"Shina O.","lastName":" Abidoye","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":true,"WBId":null,"orcid":null},{"affiliations":["University of Lagos, Lagos, Nigeria"],"departments":["Department of Microbiology"],"credit":["investigation","writing_originalDraft","writing_reviewEditing"],"email":"evansoleka6@gmail.com","firstName":"Evans C. ","lastName":"Oleka","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":true,"WBId":null,"orcid":null},{"affiliations":["University of Lagos, Lagos, Nigeria"],"departments":["Department of Microbiology"],"credit":["investigation","writing_originalDraft","writing_reviewEditing"],"email":"oluwatunkunmi@gmail.com","firstName":"Oluwatunkunmi J. ","lastName":"Okupa","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":true,"WBId":null,"orcid":null},{"affiliations":["University of Lagos, Lagos, Nigeria"],"departments":["Department of Microbiology"],"credit":["investigation","writing_originalDraft","writing_reviewEditing"],"email":"lawalfuhad51@gmail.com","firstName":"Fuhad T.","lastName":"Lawal","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":true,"WBId":null,"orcid":null},{"affiliations":["University of Lagos, Lagos, Nigeria"],"departments":["Department of Microbiology"],"credit":["investigation","writing_originalDraft","writing_reviewEditing"],"email":"immanuelgrace.o@gmail.com","firstName":"Grace O. ","lastName":"Immanuel","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":true,"WBId":null,"orcid":null},{"affiliations":["University of Lagos, Lagos, Nigeria"],"departments":["Department of Microbiology"],"credit":["investigation","writing_originalDraft","writing_reviewEditing"],"email":"emmanueltomi3264@gmail.com","firstName":"Tomi E.","lastName":"Adeyanju","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":true,"WBId":null,"orcid":null},{"affiliations":["University of Lagos, Lagos, Nigeria"],"departments":["Department of Microbiology"],"credit":["investigation","writing_originalDraft","writing_reviewEditing"],"email":"onyekachifaith0804@gmail.com","firstName":"Faith O. ","lastName":"Onyekachi","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":true,"WBId":null,"orcid":null},{"affiliations":["University of Lagos, Lagos, Nigeria"],"departments":["Department of Microbiology"],"credit":["investigation","writing_originalDraft","writing_reviewEditing"],"email":"gloriaakpederi5@gmail.com","firstName":"Omogwigho G. ","lastName":"Akpederi","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":true,"WBId":null,"orcid":null},{"affiliations":["University of Lagos, Lagos, Nigeria"],"departments":["Department of Microbiology"],"credit":["investigation","writing_originalDraft","writing_reviewEditing"],"email":"foyinsolaj@gmail.com","firstName":"Oluwafoyinsolami I. ","lastName":"Adisa","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":true,"WBId":null,"orcid":null},{"affiliations":["University of Lagos, Lagos, Nigeria"],"departments":["Department of Microbiology"],"credit":["investigation","writing_originalDraft","writing_reviewEditing"],"email":"midexy24@gmail.com","firstName":"Modesola O. ","lastName":"Onikoro","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":true,"WBId":null,"orcid":null},{"affiliations":["University of Evansville, Evansville, Indiana, United States"],"departments":["Department of Biology"],"credit":["investigation","writing_originalDraft","writing_reviewEditing"],"email":"cb508@evansville.edu","firstName":"Chase ","lastName":"Boyles","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":false,"WBId":null,"orcid":null},{"affiliations":["University of Evansville, Evansville, Indiana, United States"],"departments":["Department of Biology"],"credit":["investigation","supervision","validation","writing_originalDraft","writing_reviewEditing"],"email":"jm757@evansville.edu","firstName":"Julie A.","lastName":"Merkel","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":false,"WBId":null,"orcid":null},{"affiliations":["University of Lagos, Lagos, Nigeria"],"departments":["Department of Microbiology"],"credit":["investigation","supervision","writing_originalDraft","writing_reviewEditing"],"email":"milori@unilag.edu.ng","firstName":"Matthew O. ","lastName":"Ilori","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":false,"WBId":null,"orcid":null}],"awards":[],"conflictsOfInterest":"The authors declare that there are no conflicts of interest present.
","dataTable":{"url":null},"extendedData":[],"funding":"No funding was received to assist with the preparation of this manuscript.
","image":{"url":"https://portal.micropublication.org/uploads/e47df77b39a4d878d38641c884e58a9d.png"},"imageCaption":"Mugiwara is on the left, and CeilingFan is on the right. Plaques formed by phage Mugiwara on S. avermitilis NRRL 8165 (top). Plaques formed by phage CeilingFan on S. griseus ATCC 10137 (top). (C) Transmission electron micrograph of Mugiwara stained with 1% uranyl acetate and imaged at 120 kV, Scale bar = 75 nm (bottom). The capsid measures 79 nm, and its tail length is 348 nm, (n=1). (D) Transmission electron micrograph (TEM) of CeilingFan stained with 1% uranyl acetate using JEOL 1400 Plus and imaged with AMT8 mixpel camera at 100 kV, Scale bar = 100 nm; the capsid diameter is [62.2 nm + 4.76, (n=10)], and the tail length is [365nm + 15.6, (n=10)] (bottom).
","imageTitle":"Plaques and Transmission Electron Micrographs of Mugiwara (left), and CeilingFan (right)
","methods":"","reagents":"","patternDescription":"The continued discovery and characterization of Streptomyces bacteriophages improve our understanding of phage-host interactions, phage diversity, phage genome architecture, and their potential applications in combating antibiotic resistance. Streptomyces griseus subsp. griseus ATCC 10137 and Streptomyces avermitilis NRRL 8165 are bacterial type strains for studying the biology of Streptomyces (Hatfull, 2020; Kronheim et al., 2023; Rackow et al., 2024).
Here, we report the characteristics of CeilingFan and Mugiwara, isolated from slightly damp soil in Evansville, IN, USA (37.973088 N, 87.533631 W) and a grassy area near fir trees in Noertrange, Luxembourg (49.98127, 5.903158 E), respectively. Using standard protocols (Zorawik et al., 2024), CeilingFan was extracted by the enrichment method and Mugiwara by direct isolation. Briefly, soil samples were suspended in nutrient broth supplemented with glucose, MgCl2, and Ca (NO3)2, and the suspension was subsequently filtered using a 0.22 µm filter. The filtrate for Mugiwara was plated directly in top agar supplemented with S. avermitilis NRRL 8165, whereas the filtrate for CeilingFan was first inoculated with S. griseus ATCC 10137, incubated at 20 °C for 72h, and the resulting culture filtered before the filtrate was plated in top agar with S. griseus ATCC 10137. Plates for Mugiwara and CeilingFan were always incubated at 37 ˚C and 30 ˚C, with CeilingFan plates incubated for 48 hours. Mugiwara formed small, clear plaques (1.14 mm +0.63, n=41 (Schnieder et al., 2012)), whereas CeilingFan formed slightly larger, clear plaques (1.9 mm +0.63, n=64 (Cacciabue et al., 2019)). Both phages were purified through three rounds of plating before lysates were prepared. Transmission electron microscopy after negative staining of lysates with uranyl acetate (1%) revealed siphovirus morphology for both phages. CeilingFan has a capsid diameter of 62 nm and a tail length of 346 nm, while Mugiwara featured a larger capsid measuring 79 nm and a tail length of 348 nm (n=1) (Figure 1).
DNA was extracted from high-titer lysates of CeilingFan and Mugiwara using the Promega Wizard DNA Cleanup kit. CeilingFan and Mugiwara genomes were prepared for sequencing using the NEB Ultra II Library kit (New England Biolabs, Ipswich, MA, USA) and sequenced on the Illumina MiSeq 1000 v3 platform using the 150-bp single-end sequencing strategy at the Pittsburgh Bacteriophage Institute. Raw reads were assembled using Newbler version v3.0 (Miller et al., 2010) and checked for completeness and genomic termini using Consed v29 (Gordon et al., 1998; Russell, 2018). The number of reads generated for CeilingFan was 413,717, allowing for assembly with 466-fold coverage of a genome 132,946 bp long, with G+C content of 49.3% and a direct terminal repeat length of 12,339 bp. For Mugiwara, 342,705 reads provided 391-fold coverage of an assembled genome 133,330 bp long with G+C content of 49.1% and a direct terminal repeat length of 11,945 bp.
Auto-annotation was performed in DNA Master v 5.23.6 (http://cobamide2.bio.pitt.edu/) with Glimmer v3.02 (Delcher et al., 2007) and Genemark v2.5 (Besemer and Borodovsky, 2005), then manually refined using Starterator (http://phages.wustl.edu/starterator) for start sites comparisons (Pope and Jacobs-Sera, 2018). Functions were predicted by BLAST, using the Actinobacteriophage and NCBI non-redundant database searches v2.13.0 (Altschul et al., 1997; Russell and Hatfull, 2017), HHPRED, using the PDB_mmCIF70, (Söding, 2005), Pfam- v.36, NCBI Conserved Domains databases, Phamerator, using Actino_draft database v578 (Cresawn et al., 2011), The Observable Notebook, Subclusters (Bendele et al., 2025) and The Observable Notebook, Pham Matrices (Cobb et al., 2025). The presence of tRNAs and tmRNAs were examined using Aragorn v1.2.41 (Laslett and Canbett, 2004) and tRNAscan-SE v2.0.12 (Lowe and Eddy, 1999) and membrane proteins were identified using SOSUI v1.1 (Hirokawa et al., 1998; Mitaku & Hirokawa, 1999; Mitaku et al., 2002) and DeepTMHMM 1.0.42 (Hallgren et al., 2022). All software was used with default parameters.
Based on gene content similarity (GCS) of at least 35% to previously annotated phages within the Actinobacteriophage Database (phagesdb.org), both phages were assigned to subcluster BE2 (Russell and Hatfull, 2017; Pope et. al., 2017) and share 79% GCS with one another. CeilingFan encodes 44 predicted tRNAs, one predicted tmRNA and 248 predicted protein-coding genes, with 64 of the latter assigned putative functions; 181 genes are in the forward direction and 67 genes in the reverse direction. Mugiwara similarly encodes 44 putative tRNAs and one tmRNA and has 247 predicted protein-coding genes, of which 59 could be assigned putative functions; 183 genes are in the forward direction and 64 reverse genes.
As is typical for BE2 phages, genes encoding putative holin and endolysin proteins were identified in both CeilingFan and Mugiwara. No genes encoding a putative integrase or immunity repressor were identified in either phage, suggesting they are unlikely to establish lysogeny. MazG-like nucleotide, Ro-like RNA binding protein, DprA-like ssDNA binding protein, Cas4 exonuclease were among the functions commonly identified across BE2 phages. Mugiwara lacks the Lys-M-like peptidoglycan binding protein found in a majority of BE2 phages (23/33 phages) but it is the only BE2 member in which a putative histidine triad nucleotide binding protein has been identified. Uniquely, Mugiwara encodes a putative thioredoxin that shares little homology to the thioredoxin encoded by other BE2 phages. Similarly, CeilingFan encodes an HNH endonuclease and DNA Q-like DNA polymerase III subunit with little homology to that encoded by other BE2 phages, except for phage TomSawyer.
Nucleotide sequence accession numbers
The complete genome sequences for both phages are available at GenBank with Accession Nos. PV165877 and PV876970 and Sequence Read Archive (SRA) Nos.SRR34858420 and SRR34858425 (CeilingFan and Mugiwara respectively).
","references":[{"reference":"Altschul S. 1997. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Research 25: 3389-3402.
","pubmedId":"","doi":"10.1093/nar/25.17.3389"},{"reference":"Bendele M, Cobb I, and Cresawn S. Subclusters. Accessed August 5, 2025. Observable. https://observablehq.com/d/5e5bc78c9b3ae2ed
","pubmedId":"","doi":""},{"reference":"Besemer J, Borodovsky M. 2005. GeneMark: web software for gene finding in prokaryotes, eukaryotes and viruses. Nucleic Acids Research 33: W451-W454.
","pubmedId":"","doi":"10.1093/nar/gki487"},{"reference":"Cacciabue M, Currá A, Gismondi MI. 2019. ViralPlaque: a Fiji macro for automated assessment of viral plaque statistics. PeerJ 7: e7729.
","pubmedId":"","doi":"10.7717/peerj.7729"},{"reference":"Cobb I, Cooper K, Bendele M, Fisher R, Jones, Z, Shifflett Z, Cresawn S. Pham Matrices. Accessed August 5, 2025. Observable. https://observablehq.com/@cresawn-labs/pham-matrix.
","pubmedId":"","doi":""},{"reference":"Cresawn SG, Bogel M, Day N, Jacobs-Sera D, Hendrix RW, Hatfull GF. 2011. Phamerator: a bioinformatic tool for comparative bacteriophage genomics. BMC Bioinformatics 12: 10.1186/1471-2105-12-395.
","pubmedId":"","doi":"10.1186/1471-2105-12-395"},{"reference":"Delcher AL, Bratke KA, Powers EC, Salzberg SL. 2007. Identifying bacterial genes and endosymbiont DNA with Glimmer. Bioinformatics 23: 673-679.
","pubmedId":"","doi":"10.1093/bioinformatics/btm009"},{"reference":"Gordon D, Abajian C, Green P. 1998. Consed: A Graphical Tool for Sequence Finishing. Genome Research 8: 195-202.
","pubmedId":"","doi":"10.1101/gr.8.3.195"},{"reference":"Hallgren J, Tsirigos KD, Pedersen MD, Almagro Armenteros JJ, Marcatili P, Nielsen H, Krogh A, Winther O. 2022. DeepTMHMM predicts alpha and beta transmembrane proteins using deep neural networks. : 10.1101/2022.04.08.487609.
","pubmedId":"","doi":"10.1101/2022.04.08.487609"},{"reference":"Hatfull GF. 2020. Actinobacteriophages: Genomics, Dynamics, and Applications. Annual Review of Virology 7: 37-61.
","pubmedId":"","doi":"10.1146/annurev-virology-122019-070009"},{"reference":"Hirokawa T, Boon-Chieng S, Mitaku S. 1998. SOSUI: classification and secondary structure prediction system for membrane proteins.. Bioinformatics 14: 378-379.
","pubmedId":"","doi":"10.1093/bioinformatics/14.4.378"},{"reference":"Kronheim S, Solomon E, Ho L, Glossop M, Davidson AR, Maxwell KL. 2023. Complete genomes and comparative analyses of Streptomyces phages that influence secondary metabolism and sporulation. Scientific Reports 13: 10.1038/s41598-023-36938-z.
","pubmedId":"","doi":"10.1038/s41598-023-36938-z"},{"reference":"Laslett D. 2004. ARAGORN, a program to detect tRNA genes and tmRNA genes in nucleotide sequences. Nucleic Acids Research 32: 11-16.
","pubmedId":"","doi":"10.1093/nar/gkh152"},{"reference":"Lowe TM, Eddy SR. 1997. tRNAscan-SE: A Program for Improved Detection of Transfer RNA Genes in Genomic Sequence. Nucleic Acids Research 25: 955-964.
","pubmedId":"","doi":"10.1093/nar/25.5.955 "},{"reference":"Miller JR, Koren S, Sutton G. 2010. Assembly algorithms for next-generation sequencing data. Genomics 95: 315-327.
","pubmedId":"","doi":"10.1016/j.ygeno.2010.03.001"},{"reference":"Mitaku S, Hirokawa T. 1999. Physicochemical factors for discriminating between soluble and membrane proteins: hydrophobicity of helical segments and protein length. Protein Engineering, Design and Selection 12: 953-957.
","pubmedId":"","doi":"10.1093/protein/12.11.953"},{"reference":"Mitaku S, Hirokawa T, Tsuji T. 2002. Amphiphilicity index of polar amino acids as an aid in the\n characterization of amino acid preference at membrane–water\n interfaces. Bioinformatics 18: 608-616.
","pubmedId":"","doi":"10.1093/bioinformatics/18.4.608"},{"reference":"Pope WH, Jacobs-Sera D. 2017. Annotation of Bacteriophage Genome Sequences Using DNA Master: An Overview. Methods in Molecular Biology,Bacteriophages : 217-229.
","pubmedId":"","doi":"10.1007/978-1-4939-7343-9_16"},{"reference":"Pope WH, Mavrich TN, Garlena RA, Guerrero-Bustamante CA, Jacobs-Sera D, Montgomery MT, et al., Hatfull GF. 2017. Bacteriophages of Gordonia spp. Display a Spectrum of Diversity and Genetic Relationships. mBio 8: 10.1128/mbio.01069-17.
","pubmedId":"","doi":"10.1128/mbio.01069-17"},{"reference":"Rackow B, Rolland C, Mohnen I, Wittmann J, Müsken M, Overmann Jr, Frunzke J. 2024. Isolation and characterization of the new\n Streptomyces\n phages Kamino, Geonosis, Abafar, and Scarif infecting a broad range of host species. Microbiology Spectrum 12: 10.1128/spectrum.00663-24.
","pubmedId":"","doi":"10.1128/spectrum.00663-24"},{"reference":"Russell DA. 2018. Sequencing, assembling, and finishing complete bacteriophage genomes. Methods Mol Biol 1681:109–125.
","pubmedId":"","doi":""},{"reference":"Russell DA, Hatfull GF. 2016. PhagesDB: the actinobacteriophage database. Bioinformatics 33: 784-786.
","pubmedId":"","doi":"10.1093/bioinformatics/btw711"},{"reference":"Schneider, CA, Rasband, WS, & Eliceiri, KW. (2012). NIH Image to ImageJ: 25 years of image analysis. Nature Methods, 9(7), 671–675
","pubmedId":"","doi":"10.1038nmeth.2089"},{"reference":"Stamm J, Merkle JA, Abernathy A, Ackerman E, Brown J, Harris A, Hoffman K, Hoskins A, Jahn A, Jones N, Kitch A, Mathavan N, Rose N, Taylor J. 2024.Complete genome sequences of Streptomyces griseus phages Spelly and Phredrick. Microbiol Resour Announc13:e01049-23.https://doi.org/10.1128/mra.01049-23
","pubmedId":"","doi":"10.1128/mra.01049-23"},{"reference":"Soding J, Biegert A, Lupas AN. 2005. The HHpred interactive server for protein homology detection and structure prediction. Nucleic Acids Research 33: W244-W248.
","pubmedId":"","doi":"10.1093/nar/gki408"},{"reference":"Zorawik M, Jacobs-Sera D, Freise AC, SEA-PHAGES, Reddi K. 2024. Isolation of Bacteriophages on Actinobacteria Hosts. Methods in Molecular Biology,Phage Engineering and Analysis : 273-298.
","pubmedId":"","doi":"10.1007/978-1-0716-3798-2_17 PMID: 38526736"}],"title":"Genome Sequences of Streptomyces Cluster BE2 phages CeilingFan and Mugiwara
","reviews":[],"curatorReviews":[]},{"id":"4783e18e-72e3-48f0-ad4d-b8e62e68a785","decision":"edit","abstract":"CeilingFan and Mugiwara are novel BE2 cluster siphoviruses isolated from soil samples on Streptomyces griseus ATCC 10137 and Streptomyces avermitilis NRRL 8165, respectively. CeilingFan has a genome of 132,946 bp with 49.3% G+C content, and Mugiwara has a genome of 133,330 bp with 49.1% G+C content. Both phage genomes encode 44 tRNAs and one tmRNA. The phages are assigned to the BE2 cluster of actinobacteriophages based on gene content similarity.
","acknowledgements":"We thank members of the Howard Hughes Medical Institute Science Education Alliance-Phage Hunters Advancing Genomics and Evolutionary Science (SEA-PHAGES) program and Manuscript Data Interpretation and Nomenclature Review Team (MINT) for their support and review of the manuscript. We acknowledge Daniel French, Makayla Gomperts, and Mirkhon Normurodo at the University of Evansville who took part in the isolation of CeilingFan and University of Ottawa for isolating Mugiwara as part of their participation in the SEA-PHAGES program. We would also like to thank Dr. John Andersland (Western Kentucky University, Bowling Green, KY, USA) for providing the electron micrograph of CeilingFan.
","authors":[{"affiliations":["University of Lagos, Lagos, Nigeria"],"departments":["Department of Microbiology"],"credit":["investigation","supervision","project","validation","writing_originalDraft","writing_reviewEditing"],"email":"insa@unilag.edu.ng","firstName":"Imade Y.","lastName":"Nsa ","submittingAuthor":true,"correspondingAuthor":true,"equalContribution":false,"WBId":null,"orcid":"https://orcid.org/0000-0001-5606-268X"},{"affiliations":["University of Lagos, Lagos, Nigeria"],"departments":["Department of Microbiology"],"credit":["investigation","writing_originalDraft","writing_reviewEditing"],"email":"eziejiofor@gmail.com","firstName":"Ezichukwu E.","lastName":"Ejiofor","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":false,"WBId":null,"orcid":null},{"affiliations":["University of Lagos, Lagos, Nigeria"],"departments":["Department of Microbiology"],"credit":["investigation","writing_originalDraft","writing_reviewEditing"],"email":"ajayiemmanuel630@gmail.com","firstName":"Emmanuel T. ","lastName":"Ajayi","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":false,"WBId":null,"orcid":null},{"affiliations":["University of Lagos, Lagos, Nigeria"],"departments":["Department of Microbiology"],"credit":["investigation","writing_originalDraft","writing_reviewEditing"],"email":"okoliifunanya497@gmail.com","firstName":"Ifunanya O. ","lastName":"Okoli","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":false,"WBId":null,"orcid":null},{"affiliations":["University of Lagos, Lagos, Nigeria"],"departments":["Department of Microbiology"],"credit":["investigation","writing_originalDraft","writing_reviewEditing"],"email":"xavierchibueze@gmail.com","firstName":"Chibueze S. ","lastName":"Uchegbu","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":false,"WBId":null,"orcid":null},{"affiliations":["University of Lagos, Lagos, Nigeria"],"departments":["Department of Microbiology"],"credit":["investigation","writing_originalDraft","writing_reviewEditing"],"email":"opeoluwaaaa@gmail.com","firstName":"Opeoluwa S. ","lastName":"Aworetan","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":true,"WBId":null,"orcid":null},{"affiliations":["University of Lagos, Lagos, Nigeria"],"departments":["Department of Microbiology"],"credit":["investigation","writing_originalDraft","writing_reviewEditing"],"email":"jebfuad@gmail.com","firstName":"Fuad T.","lastName":" Jebe-Abdullah","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":true,"WBId":null,"orcid":null},{"affiliations":["University of Lagos, Lagos, Nigeria"],"departments":["Department of Microbiology"],"credit":["investigation","writing_originalDraft","writing_reviewEditing"],"email":"hauwajkam12@gmail.com","firstName":"Hauwa J.","lastName":" Kamselem","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":true,"WBId":null,"orcid":null},{"affiliations":["University of Lagos, Lagos, Nigeria"],"departments":["Department of Microbiology"],"credit":["investigation","writing_originalDraft","writing_reviewEditing"],"email":"oluwashinaabidoye@yahoo.com","firstName":"Shina O.","lastName":" Abidoye","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":true,"WBId":null,"orcid":null},{"affiliations":["University of Lagos, Lagos, Nigeria"],"departments":["Department of Microbiology"],"credit":["investigation","writing_originalDraft","writing_reviewEditing"],"email":"evansoleka6@gmail.com","firstName":"Evans C. ","lastName":"Oleka","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":true,"WBId":null,"orcid":null},{"affiliations":["University of Lagos, Lagos, Nigeria"],"departments":["Department of Microbiology"],"credit":["investigation","writing_originalDraft","writing_reviewEditing"],"email":"oluwatunkunmi@gmail.com","firstName":"Oluwatunkunmi J. ","lastName":"Okupa","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":true,"WBId":null,"orcid":null},{"affiliations":["University of Lagos, Lagos, Nigeria"],"departments":["Department of Microbiology"],"credit":["investigation","writing_originalDraft","writing_reviewEditing"],"email":"lawalfuhad51@gmail.com","firstName":"Fuhad T.","lastName":"Lawal","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":true,"WBId":null,"orcid":null},{"affiliations":["University of Lagos, Lagos, Nigeria"],"departments":["Department of Microbiology"],"credit":["investigation","writing_originalDraft","writing_reviewEditing"],"email":"immanuelgrace.o@gmail.com","firstName":"Grace O. ","lastName":"Immanuel","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":true,"WBId":null,"orcid":null},{"affiliations":["University of Lagos, Lagos, Nigeria"],"departments":["Department of Microbiology"],"credit":["investigation","writing_originalDraft","writing_reviewEditing"],"email":"emmanueltomi3264@gmail.com","firstName":"Tomi E.","lastName":"Adeyanju","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":true,"WBId":null,"orcid":null},{"affiliations":["University of Lagos, Lagos, Nigeria"],"departments":["Department of Microbiology"],"credit":["investigation","writing_originalDraft","writing_reviewEditing"],"email":"onyekachifaith0804@gmail.com","firstName":"Faith O. ","lastName":"Onyekachi","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":true,"WBId":null,"orcid":null},{"affiliations":["University of Lagos, Lagos, Nigeria"],"departments":["Department of Microbiology"],"credit":["investigation","writing_originalDraft","writing_reviewEditing"],"email":"gloriaakpederi5@gmail.com","firstName":"Omogwigho G. ","lastName":"Akpederi","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":true,"WBId":null,"orcid":null},{"affiliations":["University of Lagos, Lagos, Nigeria"],"departments":["Department of Microbiology"],"credit":["investigation","writing_originalDraft","writing_reviewEditing"],"email":"foyinsolaj@gmail.com","firstName":"Oluwafoyinsolami I. ","lastName":"Adisa","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":true,"WBId":null,"orcid":null},{"affiliations":["University of Lagos, Lagos, Nigeria"],"departments":["Department of Microbiology"],"credit":["investigation","writing_originalDraft","writing_reviewEditing"],"email":"midexy24@gmail.com","firstName":"Modesola O. ","lastName":"Onikoro","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":true,"WBId":null,"orcid":null},{"affiliations":["University of Evansville, Evansville, Indiana, United States"],"departments":["Department of Biology"],"credit":["investigation","writing_originalDraft","writing_reviewEditing"],"email":"cb508@evansville.edu","firstName":"Chase ","lastName":"Boyles","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":false,"WBId":null,"orcid":null},{"affiliations":["University of Evansville, Evansville, Indiana, United States"],"departments":["Department of Biology"],"credit":["investigation","supervision","validation","writing_originalDraft","writing_reviewEditing"],"email":"jm757@evansville.edu","firstName":"Julie A.","lastName":"Merkel","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":false,"WBId":null,"orcid":null},{"affiliations":["University of Lagos, Lagos, Nigeria"],"departments":["Department of Microbiology"],"credit":["investigation","supervision","writing_originalDraft","writing_reviewEditing"],"email":"milori@unilag.edu.ng","firstName":"Matthew O. ","lastName":"Ilori","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":false,"WBId":null,"orcid":null}],"awards":[],"conflictsOfInterest":"The authors declare that there are no conflicts of interest present.
","dataTable":{"url":null},"extendedData":[],"funding":"No funding was received to assist with the preparation of this manuscript.
","image":{"url":"https://portal.micropublication.org/uploads/a1c0d3e4a203ab2120b67fb4b8e90354.png"},"imageCaption":"Mugiwara is on the left, and CeilingFan is on the right. Plaques formed by phage Mugiwara on S. avermitilis NRRL 8165 (top). Plaques formed by phage CeilingFan on S. griseus ATCC 10137 (top). (C) Transmission electron micrograph of Mugiwara stained with 1% uranyl acetate and imaged at 120 kV, Scale bar = 75 nm (bottom). The capsid measures 79 nm, and its tail length is 348 nm, (n=1). (D) Transmission electron micrograph (TEM) of CeilingFan stained with 1% uranyl acetate using JEOL 1400 Plus and imaged with AMT8 mixpel camera at 100 kV, Scale bar = 100 nm; the capsid diameter is [62.2 nm + 4.76, (n=10)], and the tail length is [365nm + 15.6, (n=10)] (bottom).
","imageTitle":"Plaques and Transmission Electron Micrographs of Mugiwara (left), and CeilingFan (right)
","methods":"","reagents":"","patternDescription":"The continued discovery and characterization of Streptomyces bacteriophages improve our understanding of phage-host interactions, phage diversity, phage genome architecture, and their potential applications in combating antibiotic resistance. Streptomyces griseus subsp. griseus ATCC 10137 and Streptomyces avermitilis NRRL 8165 are bacterial type strains for studying the biology of Streptomyces (Hatfull, 2020; Kronheim et al., 2023; Rackow et al., 2024).
Here, we report the characteristics of CeilingFan and Mugiwara, isolated from slightly damp soil in Evansville, IN, USA (37.973088 N, 87.533631 W) and a grassy area near fir trees in Noertrange, Luxembourg (49.98127, 5.903158 E), respectively. Using standard protocols (Zorawik et al., 2024), CeilingFan was extracted by the enrichment method and Mugiwara by direct isolation. Briefly, soil samples were suspended in nutrient broth supplemented with glucose, MgCl2, and Ca (NO3)2, and the suspension was subsequently filtered using a 0.22 µm filter. The filtrate for Mugiwara was plated directly in top agar supplemented with S. avermitilis NRRL 8165, whereas the filtrate for CeilingFan was first inoculated with S. griseus ATCC 10137, incubated at 20 °C for 72h, and the resulting culture filtered before the filtrate was plated in top agar with S. griseus ATCC 10137. Plates for Mugiwara and CeilingFan were always incubated at 37 ˚C and 30 ˚C, with CeilingFan plates incubated for 48 hours. Mugiwara formed small, clear plaques (1.14 mm +0.63, n=41 (Schnieder et al., 2012)), whereas CeilingFan formed slightly larger, clear plaques (1.9 mm +0.63, n=64 (Cacciabue et al., 2019)). Both phages were purified through three rounds of plating before lysates were prepared. Transmission electron microscopy after negative staining of lysates with uranyl acetate (1%) revealed siphovirus morphology for both phages. CeilingFan has a capsid diameter of 62 nm and a tail length of 346 nm, while Mugiwara featured a larger capsid measuring 79 nm and a tail length of 348 nm (n=1) (Figure 1).
DNA was extracted from high-titer lysates of CeilingFan and Mugiwara using the Promega Wizard DNA Cleanup kit. CeilingFan and Mugiwara genomes were prepared for sequencing using the NEB Ultra II Library kit (New England Biolabs, Ipswich, MA, USA) and sequenced on the Illumina MiSeq 1000 v3 platform using the 150-bp single-end sequencing strategy at the Pittsburgh Bacteriophage Institute. Raw reads were assembled using Newbler version v3.0 (Miller et al., 2010) and checked for completeness and genomic termini using Consed v29 (Gordon et al., 1998; Russell, 2018). The number of reads generated for CeilingFan was 413,717, allowing for assembly with 466-fold coverage of a genome 132,946 bp long, with G+C content of 49.3% and a direct terminal repeat length of 12,339 bp. For Mugiwara, 342,705 reads provided 391-fold coverage of an assembled genome 133,330 bp long with G+C content of 49.1% and a direct terminal repeat length of 11,945 bp.
Auto-annotation was performed in DNA Master v 5.23.6 (http://cobamide2.bio.pitt.edu/) with Glimmer v3.02 (Delcher et al., 2007) and Genemark v2.5 (Besemer and Borodovsky, 2005), then manually refined using Starterator (http://phages.wustl.edu/starterator) for start sites comparisons (Pope and Jacobs-Sera, 2018). Functions were predicted by BLAST, using the Actinobacteriophage and NCBI non-redundant database searches v2.13.0 (Altschul et al., 1997; Russell and Hatfull, 2017), HHPRED, using the PDB_mmCIF70, (Söding, 2005), Pfam- v.36, NCBI Conserved Domains databases, Phamerator, using Actino_draft database v578 (Cresawn et al., 2011), The Observable Notebook, Subclusters (Bendele et al., 2025) and The Observable Notebook, Pham Matrices (Cobb et al., 2025). The presence of tRNAs and tmRNAs were examined using Aragorn v1.2.41 (Laslett and Canbett, 2004) and tRNAscan-SE v2.0.12 (Lowe and Eddy, 1999) and membrane proteins were identified using SOSUI v1.1 (Hirokawa et al., 1998; Mitaku & Hirokawa, 1999; Mitaku et al., 2002) and DeepTMHMM 1.0.42 (Hallgren et al., 2022). All software was used with default parameters.
Based on gene content similarity (GCS) of at least 35% to previously annotated phages within the Actinobacteriophage Database (phagesdb.org), both phages were assigned to subcluster BE2 (Russell and Hatfull, 2017; Pope et. al., 2017) and share 79% GCS with one another. CeilingFan encodes 44 predicted tRNAs, one predicted tmRNA and 248 predicted protein-coding genes, with 64 of the latter assigned putative functions; 181 genes are in the forward direction and 67 genes in the reverse direction. Mugiwara similarly encodes 44 putative tRNAs and one tmRNA and has 247 predicted protein-coding genes, of which 59 could be assigned putative functions; 183 genes are in the forward direction and 64 reverse genes.
As is typical for BE2 phages, genes encoding putative holin and endolysin proteins were identified in both CeilingFan and Mugiwara. No genes encoding a putative integrase or immunity repressor were identified in either phage, suggesting they are unlikely to establish lysogeny. MazG-like nucleotide, Ro-like RNA binding protein, DprA-like ssDNA binding protein, and Cas4 exonuclease were among the functions commonly identified across BE2 phages. Mugiwara lacks the Lys-M-like peptidoglycan binding protein found in a majority of BE2 phages (23/33 phages) but it is the only BE2 member in which a putative histidine triad nucleotide binding protein has been identified. Uniquely, Mugiwara encodes a putative thioredoxin that shares little homology to the thioredoxin encoded by other BE2 phages. Similarly, CeilingFan encodes an HNH endonuclease and DNA Q-like DNA polymerase III subunit with little homology to that encoded by other BE2 phages, except for phage TomSawyer.
Nucleotide sequence accession numbers
The complete genome sequences for both phages are available at GenBank with Accession Nos. PV165877 and PV876970 and Sequence Read Archive (SRA) Nos.SRR34858420 and SRR34858425 (CeilingFan and Mugiwara respectively).
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","pubmedId":"","doi":"10.1038nmeth.2089"},{"reference":"Stamm J, Merkle JA, Abernathy A, Ackerman E, Brown J, Harris A, Hoffman K, Hoskins A, Jahn A, Jones N, Kitch A, Mathavan N, Rose N, Taylor J. 2024.Complete genome sequences of Streptomyces griseus phages Spelly and Phredrick. Microbiol Resour Announc13:e01049-23.https://doi.org/10.1128/mra.01049-23
","pubmedId":"","doi":"10.1128/mra.01049-23"},{"reference":"Soding J, Biegert A, Lupas AN. 2005. The HHpred interactive server for protein homology detection and structure prediction. Nucleic Acids Research 33: W244-W248.
","pubmedId":"","doi":"10.1093/nar/gki408"},{"reference":"Zorawik M, Jacobs-Sera D, Freise AC, SEA-PHAGES, Reddi K. 2024. Isolation of Bacteriophages on Actinobacteria Hosts. Methods in Molecular Biology,Phage Engineering and Analysis : 273-298.
","pubmedId":"","doi":"10.1007/978-1-0716-3798-2_17 PMID: 38526736"}],"title":"Genome Sequences of Streptomyces Cluster BE2 phages CeilingFan and Mugiwara
","reviews":[],"curatorReviews":[]},{"id":"69afa6cf-70a0-4639-abd3-1152e56279b7","decision":"publish","abstract":"CeilingFan and Mugiwara are novel BE2 cluster siphoviruses isolated from soil samples on Streptomyces griseus ATCC 10137 and Streptomyces avermitilis NRRL 8165, respectively. CeilingFan has a genome of 132,946 bp with 49.3% G+C content, and Mugiwara has a genome of 133,330 bp with 49.1% G+C content. Both phage genomes encode 44 tRNAs and one tmRNA. The phages are assigned to the BE2 cluster of actinobacteriophages based on gene content similarity.
","acknowledgements":"We thank members of the Howard Hughes Medical Institute Science Education Alliance-Phage Hunters Advancing Genomics and Evolutionary Science (SEA-PHAGES) program and Manuscript Data Interpretation and Nomenclature Review Team (MINT) for their support and review of the manuscript. We acknowledge Daniel French, Makayla Gomperts, and Mirkhon Normurodo at the University of Evansville who took part in the isolation of CeilingFan and University of Ottawa for isolating Mugiwara as part of their participation in the SEA-PHAGES program. We would also like to thank Dr. John Andersland (Western Kentucky University, Bowling Green, KY, USA) for providing the electron micrograph of CeilingFan.
","authors":[{"affiliations":["University of Lagos, Lagos, Nigeria"],"departments":["Department of Microbiology"],"credit":["investigation","supervision","project","validation","writing_originalDraft","writing_reviewEditing"],"email":"insa@unilag.edu.ng","firstName":"Imade Y.","lastName":"Nsa ","submittingAuthor":true,"correspondingAuthor":true,"equalContribution":false,"WBId":null,"orcid":"https://orcid.org/0000-0001-5606-268X"},{"affiliations":["University of Lagos, Lagos, Nigeria"],"departments":["Department of Microbiology"],"credit":["investigation","writing_originalDraft","writing_reviewEditing"],"email":"eziejiofor@gmail.com","firstName":"Ezichukwu E.","lastName":"Ejiofor","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":false,"WBId":null,"orcid":null},{"affiliations":["University of Lagos, Lagos, Nigeria"],"departments":["Department of Microbiology"],"credit":["investigation","writing_originalDraft","writing_reviewEditing"],"email":"ajayiemmanuel630@gmail.com","firstName":"Emmanuel T. ","lastName":"Ajayi","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":false,"WBId":null,"orcid":null},{"affiliations":["University of Lagos, Lagos, Nigeria"],"departments":["Department of Microbiology"],"credit":["investigation","writing_originalDraft","writing_reviewEditing"],"email":"okoliifunanya497@gmail.com","firstName":"Ifunanya O. ","lastName":"Okoli","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":false,"WBId":null,"orcid":null},{"affiliations":["University of Lagos, Lagos, Nigeria"],"departments":["Department of Microbiology"],"credit":["investigation","writing_originalDraft","writing_reviewEditing"],"email":"xavierchibueze@gmail.com","firstName":"Chibueze S. ","lastName":"Uchegbu","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":false,"WBId":null,"orcid":null},{"affiliations":["University of Lagos, Lagos, Nigeria"],"departments":["Department of Microbiology"],"credit":["investigation","writing_originalDraft","writing_reviewEditing"],"email":"opeoluwaaaa@gmail.com","firstName":"Opeoluwa S. ","lastName":"Aworetan","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":true,"WBId":null,"orcid":null},{"affiliations":["University of Lagos, Lagos, Nigeria"],"departments":["Department of Microbiology"],"credit":["investigation","writing_originalDraft","writing_reviewEditing"],"email":"jebfuad@gmail.com","firstName":"Fuad T.","lastName":" Jebe-Abdullah","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":true,"WBId":null,"orcid":null},{"affiliations":["University of Lagos, Lagos, Nigeria"],"departments":["Department of Microbiology"],"credit":["investigation","writing_originalDraft","writing_reviewEditing"],"email":"hauwajkam12@gmail.com","firstName":"Hauwa J.","lastName":" Kamselem","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":true,"WBId":null,"orcid":null},{"affiliations":["University of Lagos, Lagos, Nigeria"],"departments":["Department of Microbiology"],"credit":["investigation","writing_originalDraft","writing_reviewEditing"],"email":"oluwashinaabidoye@yahoo.com","firstName":"Shina O.","lastName":" Abidoye","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":true,"WBId":null,"orcid":null},{"affiliations":["University of Lagos, Lagos, Nigeria"],"departments":["Department of Microbiology"],"credit":["investigation","writing_originalDraft","writing_reviewEditing"],"email":"evansoleka6@gmail.com","firstName":"Evans C. ","lastName":"Oleka","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":true,"WBId":null,"orcid":null},{"affiliations":["University of Lagos, Lagos, Nigeria"],"departments":["Department of Microbiology"],"credit":["investigation","writing_originalDraft","writing_reviewEditing"],"email":"oluwatunkunmi@gmail.com","firstName":"Oluwatunkunmi J. ","lastName":"Okupa","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":true,"WBId":null,"orcid":null},{"affiliations":["University of Lagos, Lagos, Nigeria"],"departments":["Department of Microbiology"],"credit":["investigation","writing_originalDraft","writing_reviewEditing"],"email":"lawalfuhad51@gmail.com","firstName":"Fuhad T.","lastName":"Lawal","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":true,"WBId":null,"orcid":null},{"affiliations":["University of Lagos, Lagos, Nigeria"],"departments":["Department of Microbiology"],"credit":["investigation","writing_originalDraft","writing_reviewEditing"],"email":"immanuelgrace.o@gmail.com","firstName":"Grace O. ","lastName":"Immanuel","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":true,"WBId":null,"orcid":null},{"affiliations":["University of Lagos, Lagos, Nigeria"],"departments":["Department of Microbiology"],"credit":["investigation","writing_originalDraft","writing_reviewEditing"],"email":"emmanueltomi3264@gmail.com","firstName":"Tomi E.","lastName":"Adeyanju","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":true,"WBId":null,"orcid":null},{"affiliations":["University of Lagos, Lagos, Nigeria"],"departments":["Department of Microbiology"],"credit":["investigation","writing_originalDraft","writing_reviewEditing"],"email":"onyekachifaith0804@gmail.com","firstName":"Faith O. ","lastName":"Onyekachi","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":true,"WBId":null,"orcid":null},{"affiliations":["University of Lagos, Lagos, Nigeria"],"departments":["Department of Microbiology"],"credit":["investigation","writing_originalDraft","writing_reviewEditing"],"email":"gloriaakpederi5@gmail.com","firstName":"Omogwigho G. ","lastName":"Akpederi","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":true,"WBId":null,"orcid":null},{"affiliations":["University of Lagos, Lagos, Nigeria"],"departments":["Department of Microbiology"],"credit":["investigation","writing_originalDraft","writing_reviewEditing"],"email":"foyinsolaj@gmail.com","firstName":"Oluwafoyinsolami I. ","lastName":"Adisa","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":true,"WBId":null,"orcid":null},{"affiliations":["University of Lagos, Lagos, Nigeria"],"departments":["Department of Microbiology"],"credit":["investigation","writing_originalDraft","writing_reviewEditing"],"email":"midexy24@gmail.com","firstName":"Modesola O. ","lastName":"Onikoro","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":true,"WBId":null,"orcid":null},{"affiliations":["University of Evansville, Evansville, Indiana, United States"],"departments":["Department of Biology"],"credit":["investigation","writing_originalDraft","writing_reviewEditing"],"email":"cb508@evansville.edu","firstName":"Chase ","lastName":"Boyles","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":false,"WBId":null,"orcid":null},{"affiliations":["University of Evansville, Evansville, Indiana, United States"],"departments":["Department of Biology"],"credit":["investigation","supervision","validation","writing_originalDraft","writing_reviewEditing"],"email":"jm757@evansville.edu","firstName":"Julie A.","lastName":"Merkle","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":false,"WBId":null,"orcid":null},{"affiliations":["University of Lagos, Lagos, Nigeria"],"departments":["Department of Microbiology"],"credit":["investigation","supervision","writing_originalDraft","writing_reviewEditing"],"email":"milori@unilag.edu.ng","firstName":"Matthew O. ","lastName":"Ilori","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":false,"WBId":null,"orcid":null}],"awards":[],"conflictsOfInterest":"The authors declare that there are no conflicts of interest present.
","dataTable":{"url":null},"extendedData":[],"funding":"No funding was received to assist with the preparation of this manuscript.
","image":{"url":"https://portal.micropublication.org/uploads/a1c0d3e4a203ab2120b67fb4b8e90354.png"},"imageCaption":"Mugiwara is on the left, and CeilingFan is on the right. Plaques formed by phage Mugiwara on S. avermitilis NRRL 8165 (top). Plaques formed by phage CeilingFan on S. griseus ATCC 10137 (top). (C) Transmission electron micrograph of Mugiwara stained with 1% uranyl acetate and imaged at 120 kV, Scale bar = 75 nm (bottom). The capsid measures 79 nm, and its tail length is 348 nm, (n=1). (D) Transmission electron micrograph (TEM) of CeilingFan stained with 1% uranyl acetate using JEOL 1400 Plus and imaged with AMT8 mixpel camera at 100 kV, Scale bar = 100 nm; the capsid diameter is [62.2 nm + 4.76, (n=10)], and the tail length is [365nm + 15.6, (n=10)] (bottom).
","imageTitle":"Plaques and Transmission Electron Micrographs of Mugiwara (left), and CeilingFan (right)
","methods":"","reagents":"","patternDescription":"The continued discovery and characterization of Streptomyces bacteriophages improve our understanding of phage-host interactions, phage diversity, phage genome architecture, and their potential applications in combating antibiotic resistance. Streptomyces griseus subsp. griseus ATCC 10137 and Streptomyces avermitilis NRRL 8165 are bacterial type strains for studying the biology of Streptomyces (Hatfull, 2020; Kronheim et al., 2023; Rackow et al., 2024).
Here, we report the characteristics of CeilingFan and Mugiwara, isolated from slightly damp soil in Evansville, IN, USA (37.973088 N, 87.533631 W) and a grassy area near fir trees in Noertrange, Luxembourg (49.98127, 5.903158 E), respectively. Using standard protocols (Zorawik et al., 2024), CeilingFan was extracted by the enrichment method and Mugiwara by direct isolation. Briefly, soil samples were suspended in nutrient broth supplemented with glucose, MgCl2, and Ca (NO3)2, and the suspension was subsequently filtered using a 0.22 µm filter. The filtrate for Mugiwara was plated directly in top agar supplemented with S. avermitilis NRRL 8165, whereas the filtrate for CeilingFan was first inoculated with S. griseus ATCC 10137, incubated at 20 °C for 72h, and the resulting culture filtered before the filtrate was plated in top agar with S. griseus ATCC 10137. Plates for Mugiwara and CeilingFan were always incubated at 37 ˚C and 30 ˚C, with CeilingFan plates incubated for 48 hours. Mugiwara formed small, clear plaques (1.14 mm +0.63, n=41 (Schnieder et al., 2012)), whereas CeilingFan formed slightly larger, clear plaques (1.9 mm +0.63, n=64 (Cacciabue et al., 2019)). Both phages were purified through three rounds of plating before lysates were prepared. Transmission electron microscopy after negative staining of lysates with uranyl acetate (1%) revealed siphovirus morphology for both phages. CeilingFan has a capsid diameter of 62 nm and a tail length of 346 nm, while Mugiwara featured a larger capsid measuring 79 nm and a tail length of 348 nm (n=1) (Figure 1).
DNA was extracted from high-titer lysates of CeilingFan and Mugiwara using the Promega Wizard DNA Cleanup kit. CeilingFan and Mugiwara genomes were prepared for sequencing using the NEB Ultra II Library kit (New England Biolabs, Ipswich, MA, USA) and sequenced on the Illumina MiSeq 1000 v3 platform using the 150-bp single-end sequencing strategy at the Pittsburgh Bacteriophage Institute. Raw reads were assembled using Newbler version v3.0 (Miller et al., 2010) and checked for completeness and genomic termini using Consed v29 (Gordon et al., 1998; Russell, 2018). The number of reads generated for CeilingFan was 413,717, allowing for assembly with 466-fold coverage of a genome 132,946 bp long, with G+C content of 49.3% and a direct terminal repeat length of 12,339 bp. For Mugiwara, 342,705 reads provided 391-fold coverage of an assembled genome 133,330 bp long with G+C content of 49.1% and a direct terminal repeat length of 11,945 bp.
Auto-annotation was performed in DNA Master v 5.23.6 (http://cobamide2.bio.pitt.edu/) with Glimmer v3.02 (Delcher et al., 2007) and Genemark v2.5 (Besemer and Borodovsky, 2005), then manually refined using Starterator (http://phages.wustl.edu/starterator) for start sites comparisons (Pope and Jacobs-Sera, 2018). Functions were predicted by BLAST, using the Actinobacteriophage and NCBI non-redundant database searches v2.13.0 (Altschul et al., 1997; Russell and Hatfull, 2017), HHPRED, using the PDB_mmCIF70, (Söding, 2005), Pfam- v.36, NCBI Conserved Domains databases, Phamerator, using Actino_draft database v578 (Cresawn et al., 2011), The Observable Notebook, Subclusters (Bendele et al., 2025) and The Observable Notebook, Pham Matrices (Cobb et al., 2025). The presence of tRNAs and tmRNAs were examined using Aragorn v1.2.41 (Laslett and Canbett, 2004) and tRNAscan-SE v2.0.12 (Lowe and Eddy, 1999) and membrane proteins were identified using SOSUI v1.1 (Hirokawa et al., 1998; Mitaku & Hirokawa, 1999; Mitaku et al., 2002) and DeepTMHMM 1.0.42 (Hallgren et al., 2022). All software was used with default parameters.
Based on gene content similarity (GCS) of at least 35% to previously annotated phages within the Actinobacteriophage Database (phagesdb.org), both phages were assigned to subcluster BE2 (Russell and Hatfull, 2017; Pope et. al., 2017) and share 79% GCS with one another. CeilingFan encodes 44 predicted tRNAs, one predicted tmRNA and 248 predicted protein-coding genes, with 64 of the latter assigned putative functions; 181 genes are in the forward direction and 67 genes in the reverse direction. Mugiwara similarly encodes 44 putative tRNAs and one tmRNA and has 247 predicted protein-coding genes, of which 59 could be assigned putative functions; 183 genes are in the forward direction and 64 reverse genes.
As is typical for BE2 phages, genes encoding putative holin and endolysin proteins were identified in both CeilingFan and Mugiwara. No genes encoding a putative integrase or immunity repressor were identified in either phage, suggesting they are unlikely to establish lysogeny. MazG-like nucleotide, Ro-like RNA binding protein, DprA-like ssDNA binding protein, and Cas4 exonuclease were among the functions commonly identified across BE2 phages. Mugiwara lacks the Lys-M-like peptidoglycan binding protein found in a majority of BE2 phages (23/33 phages) but it is the only BE2 member in which a putative histidine triad nucleotide binding protein has been identified. Uniquely, Mugiwara encodes a putative thioredoxin that shares little homology to the thioredoxin encoded by other BE2 phages. Similarly, CeilingFan encodes an HNH endonuclease and DNA Q-like DNA polymerase III subunit with little homology to that encoded by other BE2 phages, except for phage TomSawyer.
Nucleotide sequence accession numbers
The complete genome sequences for both phages are available at GenBank with Accession Nos. PV165877 and PV876970 and Sequence Read Archive (SRA) Nos.SRR34858420 and SRR34858425 (CeilingFan and Mugiwara respectively).
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","pubmedId":"","doi":"10.1007/978-1-0716-3798-2_17 PMID: 38526736"}],"title":"Genome Sequences of Streptomyces Cluster BE2 phages CeilingFan and Mugiwara
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