We report the genome sequences of four novel phages that infect Mycobacterium smegmatis mc2155. Each phage has siphoviral morphology and a double-stranded DNA genome. Based on gene content similarity, these phages belong to the K cluster of Mycobacterium phages. No novel genomic features were noted beyond those previously observed for phages of the K cluster.
","acknowledgements":"Tyler Clifton discovered and performed the initial characterization of bacteriophage TClif. We are grateful to Graham Hatfull, Deborah Jacobs-Sera, Vic Sivanathan, Billy Biederman, and the HHMI for their continuous support, quality control and revision of the manuscript, and to Daniel Russel and Becky Garlena for sequencing and assembling the phage genomes. We are thankful to John Andersland for assistance with electron microscopy.
","authors":[{"affiliations":["Western Kentucky University, Bowling Green, KY, United States"],"departments":["Biological Sciences"],"credit":["investigation","writing_reviewEditing"],"email":"ssileo1@jh.edu","firstName":"Sofia ","lastName":"Sileo","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":true,"WBId":null,"orcid":""},{"affiliations":["Western Kentucky University, Bowling Green, KY, United States"],"departments":["Biological Sciences"],"credit":["investigation","writing_reviewEditing"],"email":"danielalopezllorens2028@u.northwestern.edu","firstName":"Daniela","lastName":"Lopez Llorens","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":true,"WBId":null,"orcid":""},{"affiliations":["Western Kentucky University, Bowling Green, KY, United States"],"departments":["Biological Sciences"],"credit":["investigation","writing_reviewEditing"],"email":"alaina.bowers699@topper.wku.edu","firstName":"Alaina","lastName":"Bowers","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":true,"WBId":null,"orcid":""},{"affiliations":["Western Kentucky University, Bowling Green, KY, United States"],"departments":["Biological Sciences"],"credit":["investigation","writing_reviewEditing"],"email":"trisha.chhabra410@topper.wku.edu","firstName":"Trisha","lastName":"Chhabra","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":true,"WBId":null,"orcid":""},{"affiliations":["Western Kentucky University, Bowling Green, KY, United States"],"departments":["Biological Sciences"],"credit":["investigation","writing_reviewEditing"],"email":"natalie.clark200@topper.wku.edu","firstName":"Natalie","lastName":"Clark","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":true,"WBId":null,"orcid":""},{"affiliations":["Western Kentucky University, Bowling Green, KY, United States"],"departments":["Biological Sciences"],"credit":["investigation","writing_reviewEditing"],"email":"himani.gangumolu242@topper.wku.edu","firstName":"Himani","lastName":"Gangumolu","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":true,"WBId":null,"orcid":""},{"affiliations":["Western Kentucky University, Bowling Green, KY, United States"],"departments":["Biological Sciences"],"credit":["investigation","writing_reviewEditing"],"email":"christina.gast341@topper.wku.edu","firstName":"Lucy","lastName":"Gast","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":true,"WBId":null,"orcid":""},{"affiliations":["Western Kentucky University, Bowling Green, KY, United States"],"departments":["Biological 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University, Bowling Green, KY, United States"],"departments":["Biological Sciences"],"credit":["investigation","writing_reviewEditing"],"email":"kaylee.hutchison261@topper.wku.edu","firstName":"Kaylee","lastName":"Hutchison","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":true,"WBId":null,"orcid":""},{"affiliations":["Western Kentucky University, Bowling Green, KY, United States"],"departments":["Biological Sciences"],"credit":["investigation","writing_reviewEditing"],"email":"sanam.krishnani503@topper.wku.edu","firstName":"Sanam","lastName":"Krishnani","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":true,"WBId":null,"orcid":""},{"affiliations":["Western Kentucky University, Bowling Green, KY, United States"],"departments":["Biological 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University, Bowling Green, KY, United States"],"departments":["Biological Sciences"],"credit":["investigation","writing_reviewEditing"],"email":"shelby.spencer216@topper.wku.edu","firstName":"Shelby","lastName":"Spencer","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":true,"WBId":null,"orcid":""},{"affiliations":["Western Kentucky University, Bowling Green, KY, United States"],"departments":["Biological Sciences"],"credit":["investigation","writing_reviewEditing"],"email":"nicholas.sugimoto649@topper.wku.edu","firstName":"Nicholas","lastName":"Sugimoto","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":true,"WBId":null,"orcid":""},{"affiliations":["Western Kentucky University, Bowling Green, KY, United States"],"departments":["Biological Sciences"],"credit":["investigation","writing_reviewEditing"],"email":"simon.sy655@topper.wku.edu","firstName":"Simon","lastName":"Sy","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":true,"WBId":null,"orcid":""},{"affiliations":["Western Kentucky University, Bowling Green, KY, United States"],"departments":["Biological Sciences"],"credit":["investigation","writing_reviewEditing"],"email":"sophia.thomas795@topper.wku.edu","firstName":"Sophia","lastName":"Thomas","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":true,"WBId":null,"orcid":""},{"affiliations":["Western Kentucky University, Bowling Green, KY, United States"],"departments":["Biological Sciences"],"credit":["supervision","investigation","validation","writing�ReviewAndEditing"],"email":"claire.rinehart@wku.edu","firstName":"Claire","lastName":"A. Rinehart","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":false,"WBId":null,"orcid":""},{"affiliations":["Western Kentucky University, Bowling Green, KY, United States"],"departments":["Biological Sciences"],"credit":["supervision","investigation","validation","writingOriginalDraft","writing�ReviewAndEditing"],"email":"rodney.king@wku.edu","firstName":"Rodney","lastName":"A. King","submittingAuthor":true,"correspondingAuthor":true,"equalContribution":false,"WBId":null,"orcid":"0000-0003-2073-2965"}],"awards":[],"conflictsOfInterest":"The authors declare that there are no conflicts of interest present.
","dataTable":{"url":"https://portal.micropublication.org/uploads/1b94f6dc1cc67e3c3f29f984841ce241.csv"},"extendedData":[],"funding":"Funding was provided by the Carol Martin Gatton Academy of Mathematics and Science in Kentucky
","image":{"url":"https://portal.micropublication.org/uploads/708a9595a050a39830c1f706db37b85b.jpg"},"imageCaption":"Negative stain (1% uranyl acetate) transmission electron microscopy images show a siphovirus morphology with an icosahedral capsid and a flexible tail. See Table 1 for particle dimensions. Top row: TribleTrouble (left) and TClif (right). Bottom row: Llorens (left) and CallaLilly (right). Table: Phage characteristics, sequencing data and annotation results
","imageTitle":"Transmission electron microscopy images of phages
","methods":"","reagents":"","patternDescription":"Mycobacteriophages represent a rich source of viral genomic diversity, and their sequencing supports both fundamental biological insights and educational programs like the Science Education Alliance Phage Hunters Advancing Genomics and Evolutionary Science (SEA-PHAGES) initiative (Jordan et al., 2014). A deeper understanding of the genetic diversity of bacteriophage genomes may reveal novel genes whose products could have applications in medicine and biotechnology. The genomes of four double-stranded DNA (dsDNA)-tailed bacteriophages (TribleTrouble, Tclif, Llorens, and CallaLilly) that infect Mycobacterium smegmatis mc2155 are reported here. These phages provide additional representation of cluster K phages and facilitate comparative analyses of genome architecture, gene content, and structural features.
Phages were isolated using standard enrichment techniques (Zorawik et al., 2024). Briefly, soil samples were resuspended in Middlebrook 7H9 liquid medium, inoculated with M. smegmatis mc2155 and incubated with shaking at 30˚C. After 48 hours, the cultures were centrifuged, the supernatant was filtered (0.2 μm pore filter) and the filtrate was plated in top agar with M. smegmatis. Plates were incubated at 30˚C. All phages were purified through a minimum of three rounds of plaque assay.
Electron microscopy on negatively stained (uranyl acetate, 1%) particles revealed the phages have siphoviral morphology (Figure 1). Phage genomic DNA was extracted from a lysate using the Promega Wizard Cleanup Kit. Libraries were prepared using the NEB Ultra II FS kit, and sequenced on an Ilumina MiSeq 1000 (TribleTrouble, TClif and Llorens; v3 reagents) or a NextSeq1000 (CallaLilly; XLEAP-P1 kit). The raw reads generated on the MiSeq1000 were assembled with Newbler v2.9 to generate single contigs. The raw reads generated on the NextSeq1000 were trimmed with cutadapt 4.7 (using the option: –nextseq-trim 30) and filtered with skewer 0.2.2 (using the options: -q 20 -Q 30 -n -l 50) prior to assembly (Martin, 2011, Jiang et al., 2014, Wick et al, 2017). The genomes were checked for completeness and termini type using Consed v29 (Gordon and Green, 2013, Russell, 2017). Additional sequencing and genome details are summarized in Table 1.
Genes were predicted using Glimmer (Delcher et al., 2007), Genemark (Besemer and Borodovsky, 2005), Aragorn (Laslett and Canback, 2004) and tRNAscan-SE (Lowe and Eddy, 1997). Manual inspection and revision were performed using PECAAN (Rinehart et al, 2016). Within PECAAN, gene functions were assigned using HHPRED (Söding et al., 2005) alignment to the PDB_mmCIF70, Pfam- v.36, NCBI’s Conserved Domains databases and BLAST (Altschul et al., 1990), alignment to the NCBI nonredundant protein (National Center for Biotechnology Information) and PhagesDB (Russell and Hatfull, 2016) databases. Default settings were used for all software. Based on gene content similarity the phages were assigned to specific actinobacteriophage subclusters (Table 1). (Pope et al, 2017; Russell and Hatfull, 2016).
Functions were predicted for approximately 49% of the called genes across all four phages. Structural proteins (e.g. major capsid and tail proteins) are located in the left region of the genomes, followed by the lysis cassette, which includes the lysin A, holin, and lysin B genes. The predicted immunity repressor of all four phages belong to the same pham; a feature shared with phages known to form lysogens. (Cresawn et. al., 2011, Pope et al., 2011). Similarly, the predicted tyrosine integrases of TClif, Llorens and CallaLilly and the cluster K phages known to form lysogens all belong to the same pham. TribleTrouble encodes a predicted tyrosine integrase that belongs to a different pham, but is present in phages previously shown to establish lysogeny (e.g. Fionnbarth). Predicted DNA metabolism and replication genes are located on the right arm of the genome and nearly all of the predicted genes are transcribed in the forward direction. The exceptions include the predicted immunity repressor, a membrane protein, a secreted protein, and a tRNA gene located in the Llorens and CallaLilly genomes. Although phages tend to display high host specificity, members of the K1 subcluster have been shown to infect both fast- and slow-growing mycobacterial hosts (Pope et al., 2011).
Data availability:
GenBank and Sequence Read Archive (SRA) accession numbers are provided in Table 1
","references":[{"reference":"Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. 1990. Basic local alignment search tool. Journal of Molecular Biology 215: 403-410.
","pubmedId":"","doi":"doi.org/10.1016/ S0022-2836(05)80360-2"},{"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":"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, Green P. 2013. Consed: a graphical editor for next-generation sequencing. Bioinformatics 29: 2936-2937.
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","pubmedId":"","doi":"10.1186/1471-2105-15-182"},{"reference":"Jordan TC, Burnett SH, Carson S, Caruso SM, Clase K, DeJong RJ, et al., Hatfull. 2014. A Broadly Implementable Research Course in Phage Discovery and Genomics for First-Year Undergraduate Students. mBio 5: 10.1128/mbio.01051-13.
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","pubmedId":"","doi":"10.1093/nar/25.5.0955"},{"reference":"Martin M. 2011. Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet.journal 17: 10.
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","pubmedId":"","doi":""},{"reference":"Pope WH, Ferreira CM, Jacobs-Sera D, Benjamin RC, Davis AJ, DeJong RJ, et al., Hatfull. 2011. Cluster K Mycobacteriophages: Insights into the Evolutionary Origins of Mycobacteriophage TM4. PLoS ONE 6: e26750.
","pubmedId":"","doi":"10.1371/journal.pone.0026750"},{"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":"Rinehart, C.A, Gaffney B.L., Wood J.D., Smith J. (2016). PECAAN, a Phage Evidence Collection And Annotation Network. https://discover.kbrinsgd.org
","pubmedId":"","doi":""},{"reference":"Russell DA. 2017. Sequencing, Assembling, and Finishing Complete Bacteriophage Genomes. Methods in Molecular Biology,Bacteriophages : 109-125.
","pubmedId":"","doi":"10.1007/978-1-4939-7343-9_9 "},{"reference":"Russell DA, Hatfull GF. 2016. PhagesDB: the actinobacteriophage database. Bioinformatics 33: 784-786.
","pubmedId":"","doi":"10.1093/bioinformatics/btw711"},{"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":"Wick RR, Judd LM, Gorrie CL, Holt KE. 2017. Unicycler: Resolving bacterial genome assemblies from short and long sequencing reads. PLOS Computational Biology 13: e1005595.
","pubmedId":"","doi":"10.1371/journal.pcbi.1005595"},{"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"}],"title":"COMPLETE GENOME SEQUENCES of MYCOBACTERIOPHAGES TRIBLETROUBLE, TCLIF, LLORENS and CALLALILLY
","reviews":[{"reviewer":{"displayName":"Nancy Castro"},"openAcknowledgement":false,"status":{"submitted":true}}],"curatorReviews":[]},{"id":"e37dc9d8-1a6a-4ff1-98b1-1b825146f5fd","decision":"accept","abstract":"We report the genome sequences of four novel phages that infect Mycobacterium smegmatis mc2155. Phages TribleTrouble, TClif, Llorens and CallaLilly have siphovirus morphology and double-stranded DNA genomes consisting of 61,665bp, 61,466bp, 59,708bp and 59,631bp, respectively. Based on gene content similarity, these phages belong to the K cluster of Mycobacterium phages. No novel genomic features were noted beyond those previously observed for phages of the K cluster.
","acknowledgements":"Tyler Clifton discovered and performed the initial characterization of bacteriophage TClif. We are grateful to Graham Hatfull, Deborah Jacobs-Sera, Vic Sivanathan, Billy Biederman, and the HHMI for their continuous support, quality control and revision of the manuscript, and to Daniel Russell and Becky Garlena for sequencing and assembling the phage genomes. We are thankful to John Andersland for assistance with electron microscopy.
","authors":[{"affiliations":["Western Kentucky University, Bowling Green, KY, United States"],"departments":["Biological Sciences"],"credit":["investigation","writing_reviewEditing"],"email":"ssileo1@jh.edu","firstName":"Sofia ","lastName":"Sileo","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":true,"WBId":null,"orcid":""},{"affiliations":["Western Kentucky University, Bowling Green, KY, United States"],"departments":["Biological Sciences"],"credit":["investigation","writing_reviewEditing"],"email":"danielalopezllorens2028@u.northwestern.edu","firstName":"Daniela","lastName":"Lopez Llorens","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":true,"WBId":null,"orcid":""},{"affiliations":["Western Kentucky University, Bowling Green, KY, United States"],"departments":["Biological 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University, Bowling Green, KY, United States"],"departments":["Biological Sciences"],"credit":["investigation","writing_reviewEditing"],"email":"himani.gangumolu242@topper.wku.edu","firstName":"Himani","lastName":"Gangumolu","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":true,"WBId":null,"orcid":""},{"affiliations":["Western Kentucky University, Bowling Green, KY, United States"],"departments":["Biological Sciences"],"credit":["investigation","writing_reviewEditing"],"email":"christina.gast341@topper.wku.edu","firstName":"Lucy","lastName":"Gast","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":true,"WBId":null,"orcid":""},{"affiliations":["Western Kentucky University, Bowling Green, KY, United States"],"departments":["Biological 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Rinehart","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":false,"WBId":null,"orcid":""},{"affiliations":["Western Kentucky University, Bowling Green, KY, United States"],"departments":["Biological Sciences"],"credit":["supervision","investigation","validation","writingOriginalDraft","writing�ReviewAndEditing"],"email":"rodney.king@wku.edu","firstName":"Rodney","lastName":"A. King","submittingAuthor":true,"correspondingAuthor":true,"equalContribution":false,"WBId":null,"orcid":"0000-0003-2073-2965"}],"awards":[],"conflictsOfInterest":"The authors declare that there are no conflicts of interest present.
","dataTable":{"url":"https://portal.micropublication.org/uploads/1b94f6dc1cc67e3c3f29f984841ce241.csv"},"extendedData":[],"funding":"Funding was provided by the Carol Martin Gatton Academy of Mathematics and Science in Kentucky
","image":{"url":"https://portal.micropublication.org/uploads/708a9595a050a39830c1f706db37b85b.jpg"},"imageCaption":"Negative stain (1% uranyl acetate) transmission electron microscopy images show a siphovirus morphology with an icosahedral capsid and a flexible tail. See Table 1 for particle dimensions. Top row: TribleTrouble (left) and TClif (right). Bottom row: Llorens (left) and CallaLilly (right). Table: Phage characteristics, sequencing data and annotation results
","imageTitle":"Transmission electron microscopy images of phages
","methods":"","reagents":"","patternDescription":"Mycobacteriophages represent a rich source of viral genomic diversity, and their sequencing supports both fundamental biological insights and educational programs like the Science Education Alliance Phage Hunters Advancing Genomics and Evolutionary Science (SEA-PHAGES) initiative (Jordan et al., 2014). A deeper understanding of the genetic diversity of bacteriophage genomes may reveal novel genes whose products could have applications in medicine and biotechnology. The genomes of four double-stranded DNA (dsDNA)-tailed bacteriophages (TribleTrouble, TClif, Llorens, and CallaLilly) that infect Mycobacterium smegmatis mc2155 are reported here. These phages provide additional representation of cluster K phages and facilitate comparative analyses of genome architecture, gene content, and structural features.
Phages were isolated using standard enrichment techniques (Zorawik et al., 2024). Briefly, soil samples were resuspended in Middlebrook 7H9 liquid medium, inoculated with M. smegmatis mc2155 and incubated with shaking at 30˚C. After 48 hours, the cultures were centrifuged, the supernatant was filtered (0.2 μm pore filter) and the filtrate was plated in top agar with M. smegmatis. Plates were incubated at 30˚C for 48 hours. All phages were purified through a minimum of three rounds of plaque assay.
Electron microscopy on negatively stained (uranyl acetate, 1%) particles revealed the phages have siphovirus morphology (Figure 1). Phage genomic DNA was extracted from a lysate using the Promega Wizard Cleanup Kit. Libraries were prepared using the NEB Ultra II FS kit, and sequenced on an Ilumina MiSeq 1000 (TribleTrouble, TClif and Llorens; v3 reagents) or a NextSeq1000 (CallaLilly; XLEAP-P1 kit). The raw reads generated on the MiSeq1000 were assembled with Newbler v2.9 to generate single contigs. The raw reads generated on the NextSeq1000 were trimmed with cutadapt 4.7 (using the option: –nextseq-trim 30) and filtered with skewer 0.2.2 (using the options: -q 20 -Q 30 -n -l 50) prior to assembly (Martin, 2011, Jiang et al., 2014, Wick et al, 2017). The genomes were checked for completeness and termini type using Consed v29 (Gordon and Green, 2013, Russell, 2017). Additional sequencing and genome details are summarized in Table 1.
Genes were predicted using Glimmer v3.02 (Delcher et al., 2007), Genemark.hmm v3.36, GenemarkS v4.28 (Besemer and Borodovsky, 2005), Aragorn v1.2.38 (Laslett and Canback, 2004) and tRNAscan-SE v2.0.12 (Lowe and Eddy, 1997). Manual inspection and revision were performed using PECAAN v20250130 (Rinehart et al, 2016). Within PECAAN, gene functions were assigned using HHPRED (Söding et al., 2005) alignment to the PDB_mmCIF70, Pfam- v.36, NCBI’s Conserved Domains databases and BLAST (Altschul et al., 1990), alignment to the NCBI nonredundant protein (National Center for Biotechnology Information) and PhagesDB (Russell and Hatfull, 2016) databases. Default settings were used for all software. Based on gene content similarity the phages were assigned to specific actinobacteriophage subclusters (Table 1) (Pope et al, 2017; Russell and Hatfull, 2016).
Functions were predicted for approximately 49% of the called genes across all four phages. Structural proteins (e.g. major capsid and tail proteins) are located in the left region of the genomes, followed by the lysis cassette, which includes the lysin A, holin, and lysin B genes. The predicted immunity repressor of all four phages belong to the same pham; a feature shared with phages known to form lysogens. (Cresawn et. al., 2011, Pope et al., 2011). Similarly, the predicted tyrosine integrases of TClif, Llorens and CallaLilly and the cluster K phages known to form lysogens all belong to the same pham. TribleTrouble encodes a predicted tyrosine integrase that belongs to a different pham, but is present in phages previously shown to establish lysogeny (e.g. Fionnbharth). Predicted DNA metabolism and replication genes are located on the right arm of the genome and nearly all of the predicted genes are transcribed in the forward direction. The exceptions include the predicted immunity repressor, a membrane protein, a secreted protein, and a tRNA gene located in the Llorens and CallaLilly genomes. Although phages tend to display high host specificity, members of the K1 subcluster have been shown to infect both fast- and slow-growing mycobacterial hosts (Pope et al., 2011).
Data availability:
GenBank and Sequence Read Archive (SRA) accession numbers are provided in Table 1
","references":[{"reference":"Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. 1990. Basic local alignment search tool. Journal of Molecular Biology 215: 403-410.
","pubmedId":"","doi":"doi.org/10.1016/ S0022-2836(05)80360-2"},{"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":"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, Green P. 2013. Consed: a graphical editor for next-generation sequencing. Bioinformatics 29: 2936-2937.
","pubmedId":"","doi":"10.1093/bioinformatics/btt515"},{"reference":"Jiang H, Lei R, Ding SW, Zhu S. 2014. Skewer: a fast and accurate adapter trimmer for next-generation sequencing paired-end reads. BMC Bioinformatics 15: 10.1186/1471-2105-15-182.
","pubmedId":"","doi":"10.1186/1471-2105-15-182"},{"reference":"Jordan TC, Burnett SH, Carson S, Caruso SM, Clase K, DeJong RJ, et al., Hatfull. 2014. A Broadly Implementable Research Course in Phage Discovery and Genomics for First-Year Undergraduate Students. mBio 5: 10.1128/mbio.01051-13.
","pubmedId":"","doi":"10.1128/mBio.01051-13"},{"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/25.5.0955"},{"reference":"Martin M. 2011. Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet.journal 17: 10.
","pubmedId":"","doi":"10.14806/ej.17.1.200"},{"reference":"National Center for Biotechnology Information (NCBI)[Internet]. Bethesda (MD): National Library of Medicine (US), National Center for Biotechnology Information; [1988] – [cited 2024 Sept 29]. Available from: https://www.ncbi.nlm.nih.gov/
","pubmedId":"","doi":""},{"reference":"Pope WH, Ferreira CM, Jacobs-Sera D, Benjamin RC, Davis AJ, DeJong RJ, et al., Hatfull. 2011. Cluster K Mycobacteriophages: Insights into the Evolutionary Origins of Mycobacteriophage TM4. PLoS ONE 6: e26750.
","pubmedId":"","doi":"10.1371/journal.pone.0026750"},{"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":"Rinehart, C.A, Gaffney B.L., Wood J.D., Smith J. (2016). PECAAN, a Phage Evidence Collection And Annotation Network. https://discover.kbrinsgd.org
","pubmedId":"","doi":""},{"reference":"Russell DA. 2017. Sequencing, Assembling, and Finishing Complete Bacteriophage Genomes. Methods in Molecular Biology,Bacteriophages : 109-125.
","pubmedId":"","doi":"10.1007/978-1-4939-7343-9_9 "},{"reference":"Russell DA, Hatfull GF. 2016. PhagesDB: the actinobacteriophage database. Bioinformatics 33: 784-786.
","pubmedId":"","doi":"10.1093/bioinformatics/btw711"},{"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":"Wick RR, Judd LM, Gorrie CL, Holt KE. 2017. Unicycler: Resolving bacterial genome assemblies from short and long sequencing reads. PLOS Computational Biology 13: e1005595.
","pubmedId":"","doi":"10.1371/journal.pcbi.1005595"},{"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"}],"title":"Complete Genome Sequences of Mycobacteriophages TribleTrouble, TClif, Llorens and CallaLilly
","reviews":[],"curatorReviews":[]},{"id":"833496d1-348e-475d-ba3d-d4601b33939a","decision":"publish","abstract":"We report the genome sequences of four novel phages that infect Mycobacterium smegmatis mc2155. Phages TribleTrouble, TClif, Llorens and CallaLilly have siphovirus morphology and double-stranded DNA genomes consisting of 61,665bp, 61,466bp, 59,708bp and 59,631bp, respectively. Based on gene content similarity, these phages belong to the K cluster of Mycobacterium phages. No novel genomic features were noted beyond those previously observed for phages of the K cluster.
","acknowledgements":"Tyler Clifton discovered and performed the initial characterization of bacteriophage TClif. We are grateful to Graham Hatfull, Deborah Jacobs-Sera, Vic Sivanathan, Billy Biederman, and the HHMI for their continuous support, quality control and revision of the manuscript, and to Daniel Russell and Becky Garlena for sequencing and assembling the phage genomes. We are thankful to John Andersland for assistance with electron microscopy.
","authors":[{"affiliations":["Western Kentucky University, Bowling Green, KY, United States"],"departments":["Biological Sciences"],"credit":["investigation","writing_reviewEditing"],"email":"ssileo1@jh.edu","firstName":"Sofia ","lastName":"Sileo","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":true,"WBId":null,"orcid":""},{"affiliations":["Western Kentucky University, Bowling Green, KY, United States"],"departments":["Biological Sciences"],"credit":["investigation","writing_reviewEditing"],"email":"danielalopezllorens2028@u.northwestern.edu","firstName":"Daniela","lastName":"Lopez Llorens","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":true,"WBId":null,"orcid":""},{"affiliations":["Western Kentucky University, Bowling Green, KY, United States"],"departments":["Biological Sciences"],"credit":["investigation","writing_reviewEditing"],"email":"alaina.bowers699@topper.wku.edu","firstName":"Alaina","lastName":"Bowers","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":true,"WBId":null,"orcid":""},{"affiliations":["Western Kentucky University, Bowling Green, KY, United States"],"departments":["Biological Sciences"],"credit":["investigation","writing_reviewEditing"],"email":"trisha.chhabra410@topper.wku.edu","firstName":"Trisha","lastName":"Chhabra","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":true,"WBId":null,"orcid":""},{"affiliations":["Western Kentucky University, Bowling Green, KY, United States"],"departments":["Biological Sciences"],"credit":["investigation","writing_reviewEditing"],"email":"natalie.clark200@topper.wku.edu","firstName":"Natalie","lastName":"Clark","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":true,"WBId":null,"orcid":""},{"affiliations":["Western Kentucky University, Bowling Green, KY, United States"],"departments":["Biological Sciences"],"credit":["investigation","writing_reviewEditing"],"email":"himani.gangumolu242@topper.wku.edu","firstName":"Himani","lastName":"Gangumolu","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":true,"WBId":null,"orcid":""},{"affiliations":["Western Kentucky University, Bowling Green, KY, United States"],"departments":["Biological Sciences"],"credit":["investigation","writing_reviewEditing"],"email":"christina.gast341@topper.wku.edu","firstName":"Lucy","lastName":"Gast","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":true,"WBId":null,"orcid":""},{"affiliations":["Western Kentucky University, Bowling Green, KY, United States"],"departments":["Biological Sciences"],"credit":["investigation","writing_reviewEditing"],"email":"madison.gicale881@topper.wku.edu","firstName":"Madison","lastName":"Gicale","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":true,"WBId":null,"orcid":""},{"affiliations":["Western Kentucky University, Bowling Green, KY, United States"],"departments":["Biological Sciences"],"credit":["investigation","writing_reviewEditing"],"email":"vidhi.grover144@topper.wku.edu","firstName":"Vidhi","lastName":"Grover","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":true,"WBId":null,"orcid":""},{"affiliations":["Western Kentucky University, Bowling Green, KY, United States"],"departments":["Biological Sciences"],"credit":["investigation","writing_reviewEditing"],"email":"roby.hardesty701@topper.wku.edu","firstName":"Roby","lastName":"Hardesty","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":true,"WBId":null,"orcid":""},{"affiliations":["Western Kentucky University, Bowling Green, KY, United States"],"departments":["Biological Sciences"],"credit":["investigation","writing_reviewEditing"],"email":"kaylee.hutchison261@topper.wku.edu","firstName":"Kaylee","lastName":"Hutchison","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":true,"WBId":null,"orcid":""},{"affiliations":["Western Kentucky University, Bowling Green, KY, United States"],"departments":["Biological Sciences"],"credit":["investigation","writing_reviewEditing"],"email":"sanam.krishnani503@topper.wku.edu","firstName":"Sanam","lastName":"Krishnani","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":true,"WBId":null,"orcid":""},{"affiliations":["Western Kentucky University, Bowling Green, KY, United States"],"departments":["Biological Sciences"],"credit":["investigation","writing_reviewEditing"],"email":"landon.patton629@topper.wku.edu","firstName":"Landon","lastName":"Patton","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":true,"WBId":null,"orcid":""},{"affiliations":["Western Kentucky University, Bowling Green, KY, United States"],"departments":["Biological Sciences"],"credit":["investigation","writing_reviewEditing"],"email":"logan.robinson812@topper.wku.edu","firstName":"Logan","lastName":"Robinson","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":true,"WBId":null,"orcid":""},{"affiliations":["Western Kentucky University, Bowling Green, KY, United States"],"departments":["Biological Sciences"],"credit":["investigation","writing_reviewEditing"],"email":"amelia.sheehan737@topper.wku.edu","firstName":"Ash","lastName":"Sheehan","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":true,"WBId":null,"orcid":""},{"affiliations":["Western Kentucky University, Bowling Green, KY, United States"],"departments":["Biological Sciences"],"credit":["investigation","writing_reviewEditing"],"email":"shelby.spencer216@topper.wku.edu","firstName":"Shelby","lastName":"Spencer","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":true,"WBId":null,"orcid":""},{"affiliations":["Western Kentucky University, Bowling Green, KY, United States"],"departments":["Biological Sciences"],"credit":["investigation","writing_reviewEditing"],"email":"nicholas.sugimoto649@topper.wku.edu","firstName":"Nicholas","lastName":"Sugimoto","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":true,"WBId":null,"orcid":""},{"affiliations":["Western Kentucky University, Bowling Green, KY, United States"],"departments":["Biological Sciences"],"credit":["investigation","writing_reviewEditing"],"email":"simon.sy655@topper.wku.edu","firstName":"Simon","lastName":"Sy","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":true,"WBId":null,"orcid":""},{"affiliations":["Western Kentucky University, Bowling Green, KY, United States"],"departments":["Biological Sciences"],"credit":["investigation","writing_reviewEditing"],"email":"sophia.thomas795@topper.wku.edu","firstName":"Sophia","lastName":"Thomas","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":true,"WBId":null,"orcid":""},{"affiliations":["Western Kentucky University, Bowling Green, KY, United States"],"departments":["Biological Sciences"],"credit":["supervision","investigation","validation","writing_reviewEditing"],"email":"claire.rinehart@wku.edu","firstName":"Claire","lastName":"A. Rinehart","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":false,"WBId":null,"orcid":""},{"affiliations":["Western Kentucky University, Bowling Green, KY, United States"],"departments":["Biological Sciences"],"credit":["supervision","investigation","validation","writing_originalDraft","writing_reviewEditing"],"email":"rodney.king@wku.edu","firstName":"Rodney","lastName":"A. King","submittingAuthor":true,"correspondingAuthor":true,"equalContribution":false,"WBId":null,"orcid":"0000-0003-2073-2965"}],"awards":[],"conflictsOfInterest":"The authors declare that there are no conflicts of interest present.
","dataTable":{"url":"https://portal.micropublication.org/uploads/1b94f6dc1cc67e3c3f29f984841ce241.csv"},"extendedData":[],"funding":"Funding was provided by the Carol Martin Gatton Academy of Mathematics and Science in Kentucky
","image":{"url":"https://portal.micropublication.org/uploads/708a9595a050a39830c1f706db37b85b.jpg"},"imageCaption":"Negative stain (1% uranyl acetate) transmission electron microscopy images show a siphovirus morphology with an icosahedral capsid and a flexible tail. See Table 1 for particle dimensions. Top row: TribleTrouble (left) and TClif (right). Bottom row: Llorens (left) and CallaLilly (right). Table: Phage characteristics, sequencing data and annotation results
","imageTitle":"Transmission electron microscopy images of phages
","methods":"","reagents":"","patternDescription":"Mycobacteriophages represent a rich source of viral genomic diversity, and their sequencing supports both fundamental biological insights and educational programs like the Science Education Alliance Phage Hunters Advancing Genomics and Evolutionary Science (SEA-PHAGES) initiative (Jordan et al., 2014). A deeper understanding of the genetic diversity of bacteriophage genomes may reveal novel genes whose products could have applications in medicine and biotechnology. The genomes of four double-stranded DNA (dsDNA)-tailed bacteriophages (TribleTrouble, TClif, Llorens, and CallaLilly) that infect Mycobacterium smegmatis mc2155 are reported here. These phages provide additional representation of cluster K phages and facilitate comparative analyses of genome architecture, gene content, and structural features.
Phages were isolated using standard enrichment techniques (Zorawik et al., 2024). Briefly, soil samples were resuspended in Middlebrook 7H9 liquid medium, inoculated with M. smegmatis mc2155 and incubated with shaking at 30˚C. After 48 hours, the cultures were centrifuged, the supernatant was filtered (0.2 μm pore filter) and the filtrate was plated in top agar with M. smegmatis. Plates were incubated at 30˚C for 48 hours. All phages were purified through a minimum of three rounds of plaque assay.
Electron microscopy on negatively stained (uranyl acetate, 1%) particles revealed the phages have siphovirus morphology (Figure 1). Phage genomic DNA was extracted from a lysate using the Promega Wizard Cleanup Kit. Libraries were prepared using the NEB Ultra II FS kit, and sequenced on an Ilumina MiSeq 1000 (TribleTrouble, TClif and Llorens; v3 reagents) or a NextSeq1000 (CallaLilly; XLEAP-P1 kit). The raw reads generated on the MiSeq1000 were assembled with Newbler v2.9 to generate single contigs. The raw reads generated on the NextSeq1000 were trimmed with cutadapt 4.7 (using the option: –nextseq-trim 30) and filtered with skewer 0.2.2 (using the options: -q 20 -Q 30 -n -l 50) prior to assembly (Martin, 2011, Jiang et al., 2014, Wick et al, 2017). The genomes were checked for completeness and termini type using Consed v29 (Gordon and Green, 2013, Russell, 2017). Additional sequencing and genome details are summarized in Table 1.
Genes were predicted using Glimmer v3.02 (Delcher et al., 2007), Genemark.hmm v3.36, GenemarkS v4.28 (Besemer and Borodovsky, 2005), Aragorn v1.2.38 (Laslett and Canback, 2004) and tRNAscan-SE v2.0.12 (Lowe and Eddy, 1997). Manual inspection and revision were performed using PECAAN v20250130 (Rinehart et al, 2016). Within PECAAN, gene functions were assigned using HHPRED (Söding et al., 2005) alignment to the PDB_mmCIF70, Pfam- v.36, NCBI’s Conserved Domains databases and BLAST (Altschul et al., 1990), alignment to the NCBI nonredundant protein (National Center for Biotechnology Information) and PhagesDB (Russell and Hatfull, 2016) databases. Default settings were used for all software. Based on gene content similarity the phages were assigned to specific actinobacteriophage subclusters (Table 1) (Pope et al, 2017; Russell and Hatfull, 2016).
Functions were predicted for approximately 49% of the called genes across all four phages. Structural proteins (e.g. major capsid and tail proteins) are located in the left region of the genomes, followed by the lysis cassette, which includes the lysin A, holin, and lysin B genes. The predicted immunity repressor of all four phages belong to the same pham; a feature shared with phages known to form lysogens. (Cresawn et. al., 2011, Pope et al., 2011). Similarly, the predicted tyrosine integrases of TClif, Llorens and CallaLilly and the cluster K phages known to form lysogens all belong to the same pham. TribleTrouble encodes a predicted tyrosine integrase that belongs to a different pham, but is present in phages previously shown to establish lysogeny (e.g. Fionnbharth). Predicted DNA metabolism and replication genes are located on the right arm of the genome and nearly all of the predicted genes are transcribed in the forward direction. The exceptions include the predicted immunity repressor, a membrane protein, a secreted protein, and a tRNA gene located in the Llorens and CallaLilly genomes. Although phages tend to display high host specificity, members of the K1 subcluster have been shown to infect both fast- and slow-growing mycobacterial hosts (Pope et al., 2011).
Data availability:
GenBank and Sequence Read Archive (SRA) accession numbers are provided in Table 1
","references":[{"reference":"Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. 1990. Basic local alignment search tool. Journal of Molecular Biology 215: 403-410.
","pubmedId":"","doi":"doi.org/10.1016/ S0022-2836(05)80360-2"},{"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":"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, Green P. 2013. Consed: a graphical editor for next-generation sequencing. Bioinformatics 29: 2936-2937.
","pubmedId":"","doi":"10.1093/bioinformatics/btt515"},{"reference":"Jiang H, Lei R, Ding SW, Zhu S. 2014. Skewer: a fast and accurate adapter trimmer for next-generation sequencing paired-end reads. BMC Bioinformatics 15: 10.1186/1471-2105-15-182.
","pubmedId":"","doi":"10.1186/1471-2105-15-182"},{"reference":"Jordan TC, Burnett SH, Carson S, Caruso SM, Clase K, DeJong RJ, et al., Hatfull. 2014. A Broadly Implementable Research Course in Phage Discovery and Genomics for First-Year Undergraduate Students. mBio 5: 10.1128/mbio.01051-13.
","pubmedId":"","doi":"10.1128/mBio.01051-13"},{"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/25.5.0955"},{"reference":"Martin M. 2011. Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet.journal 17: 10.
","pubmedId":"","doi":"10.14806/ej.17.1.200"},{"reference":"National Center for Biotechnology Information (NCBI)[Internet]. Bethesda (MD): National Library of Medicine (US), National Center for Biotechnology Information; [1988] – [cited 2024 Sept 29]. Available from: https://www.ncbi.nlm.nih.gov/
","pubmedId":"","doi":""},{"reference":"Pope WH, Ferreira CM, Jacobs-Sera D, Benjamin RC, Davis AJ, DeJong RJ, et al., Hatfull. 2011. Cluster K Mycobacteriophages: Insights into the Evolutionary Origins of Mycobacteriophage TM4. PLoS ONE 6: e26750.
","pubmedId":"","doi":"10.1371/journal.pone.0026750"},{"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":"Rinehart, C.A, Gaffney B.L., Wood J.D., Smith J. (2016). PECAAN, a Phage Evidence Collection And Annotation Network. https://discover.kbrinsgd.org
","pubmedId":"","doi":""},{"reference":"Russell DA. 2017. Sequencing, Assembling, and Finishing Complete Bacteriophage Genomes. Methods in Molecular Biology,Bacteriophages : 109-125.
","pubmedId":"","doi":"10.1007/978-1-4939-7343-9_9 "},{"reference":"Russell DA, Hatfull GF. 2016. PhagesDB: the actinobacteriophage database. Bioinformatics 33: 784-786.
","pubmedId":"","doi":"10.1093/bioinformatics/btw711"},{"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":"Wick RR, Judd LM, Gorrie CL, Holt KE. 2017. Unicycler: Resolving bacterial genome assemblies from short and long sequencing reads. PLOS Computational Biology 13: e1005595.
","pubmedId":"","doi":"10.1371/journal.pcbi.1005595"},{"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"}],"title":"Complete Genome Sequences of Mycobacteriophages TribleTrouble, TClif, Llorens and CallaLilly
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