1887

Abstract

In an genomics course sponsored by the Howard Hughes Medical Institute (HHMI), undergraduate students have isolated and sequenced the genomes of more than 1,150 mycobacteriophages, creating the largest database of sequenced bacteriophages able to infect a single host, Mycobacterium smegmatis, a soil bacterium. Genomic analysis indicates that these mycobacteriophages can be grouped into 26 clusters based on genetic similarity. These clusters span a continuum of genetic diversity, with extensive genomic mosaicism among phages in different clusters. However, little is known regarding the primary hosts of these mycobacteriophages in their natural habitats, nor of their broader host ranges. As such, it is possible that the primary host of many newly isolated mycobacteriophages is not M. smegmatis, but instead a range of closely related bacterial species. However, determining mycobacteriophage host range presents difficulties associated with mycobacterial cultivability, pathogenicity and growth. Another way to gain insight into mycobacteriophage host range and ecology is through bioinformatic analysis of their genomic sequences. To this end, we examined the correlations between the codon usage biases of 199 different mycobacteriophages and those of several fully sequenced mycobacterial species in order to gain insight into the natural host range of these mycobacteriophages. We find that UPGMA clustering tends to match, but not consistently, clustering by shared nucleotide sequence identify. In addition, analysis of GC content, tRNA usage and correlations between mycobacteriophage and mycobacterial codon usage bias suggests that the preferred host of many clustered mycobacteriophages is not M. smegmatis but other, as yet unknown, members of the mycobacteria complex or closely allied bacterial species.

Loading

Article metrics loading...

/content/journal/mgen/10.1099/mgen.0.000079
2016-10-01
2024-03-29
Loading full text...

Full text loading...

/deliver/fulltext/mgen/2/10/mgen000079.html?itemId=/content/journal/mgen/10.1099/mgen.0.000079&mimeType=html&fmt=ahah

References

  1. Andersson G. E., Sharp P. M. 1996; Codon usage in the Mycobacterium tuberculosis complex. Microbiol 142:915–925 [View Article][PubMed]
    [Google Scholar]
  2. Bahir I., Fromer M., Prat Y., Linial M. 2009; Viral adaptation to host: a proteome-based analysis of codon usage and amino acid preferences. Mol Syst Biol 5:311 [View Article][PubMed]
    [Google Scholar]
  3. Bailly-Bechet M., Vergassola M., Rocha E. 2007; Causes for the intriguing presence of tRNAs in phages. Genome Res 17:1486–1495 [View Article][PubMed]
    [Google Scholar]
  4. Basra S., Anany H., Brovko L., Kropinski A. M., Griffiths M. W. 2014; Isolation and characterization of a novel bacteriophage against Mycobacterium avium subspecies paratuberculosis . Arch Virol 159:2659–2674 [View Article][PubMed]
    [Google Scholar]
  5. Bentley S. D., Parkhill J. 2004; Comparative genomic structure of prokaryotes. Annu Rev Genet 38:771–792 [View Article][PubMed]
    [Google Scholar]
  6. Bhat R. M., Prakash C. 2012; Leprosy: an overview of pathophysiology. Interdiscip Perspect Infect Dis 2012:181089 [View Article][PubMed]
    [Google Scholar]
  7. Bohlin J., Snipen L., Hardy S. P., Kristoffersen A. B., Lagesen K., Dønsvik T., Skjerve E., Ussery D. W. 2010; Analysis of intra-genomic GC content homogeneity within prokaryotes. BMC Genomics 11:464 [View Article][PubMed]
    [Google Scholar]
  8. Brosch R., Gordon S. V., Garnier T., Eiglmeier K., Frigui W., Valenti P., Dos Santos S., Duthoy S., Lacroix C. et al. 2007; Genome plasticity of BCG and impact on vaccine efficacy. Proc Natl Acad Sci USA 104:5596–5601 [View Article]
    [Google Scholar]
  9. Brüssow H., Hendrix R. W. 2002; Phage genomics: small is beautiful. Cell 108:13–16[PubMed]
    [Google Scholar]
  10. Carbone A. 2008; Codon bias is a major factor explaining phage evolution in translationally biased hosts. J Mol Evol 66:210–223 [View Article][PubMed]
    [Google Scholar]
  11. Chithambaram S., Prabhakaran R., Xia X. 2014; Differential codon adaptation between dsDNA and ssDNA phages in Escherichia coli . Mol Biol Evol 31:1606–1617 [View Article][PubMed]
    [Google Scholar]
  12. Cole S. T., Eiglmeier K., Parkhill J., James K. D., Thomson N. R., Wheeler P. R., Honoré N., Garnier T., Churcher C. et al. 2001; Massive gene decay in the leprosy bacillus. Nature 409:1007–1011 [View Article][PubMed]
    [Google Scholar]
  13. Cole S. T., Brosch R., Parkhill J., Garnier T., Churcher C., Harris D., Gordon S. V., Eiglmeier K., Gas S. et al. 1998; Deciphering the biology of Mycobacterium tuberculosis from the complete genome sequence. Nature 393:537–544 [View Article][PubMed]
    [Google Scholar]
  14. Colson P., Fournous G., Diene S. M., Raoult D. 2013; Codon usage, amino acid usage, transfer RNA and amino-acyl-tRNA synthetases in Mimiviruses. Intervirology 56:364–375 [View Article][PubMed]
    [Google Scholar]
  15. Cresawn S. G., Bogel M., Day N., Jacobs-Sera D., Hendrix R. W., Hatfull G. F. 2011; Phamerator: a bioinformatic tool for comparative bacteriophage genomics. BMC Bioinformatics 12:395 [View Article][PubMed]
    [Google Scholar]
  16. Dennehy J. J. 2009; Bacteriophages as model organisms for virus emergence research. Trends Microbiol 17:450–457 [View Article][PubMed]
    [Google Scholar]
  17. Dennehy J. J. 2014; What ecologists can tell virologists. Annu Rev Microbiol 68:117–135 [View Article][PubMed]
    [Google Scholar]
  18. Fierer N., Jackson R. B. 2006; The diversity and biogeography of soil bacterial communities. Proc Natl Acad Sci U S A 103:626–631 [View Article][PubMed]
    [Google Scholar]
  19. Foerstner K. U., von Mering C., Hooper S. D., Bork P. 2005; Environments shape the nucleotide composition of genomes. EMBO Rep 6:1208–1213 [View Article][PubMed]
    [Google Scholar]
  20. Gallien S., Perrodou E., Carapito C., Deshayes C., Reyrat J.-M., Van Dorsselaer A., Poch O., Schaeffer C., Lecompte O. et al. 2010; Ortho-proteogenomics: Multiple proteomes investigation through orthology and a new MS-based protocol. Genome Research 19:128–135 [View Article]
    [Google Scholar]
  21. Gao B., Gupta R. S. 2012; Phylogenetic framework and molecular signatures for the main clades of the phylum Actinobacteria . Microbiol Mol Biol Rev 76:66–112 [View Article][PubMed]
    [Google Scholar]
  22. Garcia-Vallvé S., Palau J., Romeu A. 1999; Horizontal gene transfer in glycosyl hydrolases inferred from codon usage in Escherichia coli and Bacillus subtilis . Mol Biol Evol 16:1125–1134 [View Article][PubMed]
    [Google Scholar]
  23. Grose J. H., Casjens S. R. 2014; Understanding the enormous diversity of bacteriophages: the tailed phages that infect the bacterial family Enterobacteriaceae . Virology 468-470:421–443 [View Article][PubMed]
    [Google Scholar]
  24. Hatfull G. F. Science Education Alliance Phage Hunters Advancing Genomics and Evolutionary Science (SEA-PHAGES) Program, KwaZulu-Natal Research Institute for Tuberculosis and HIV (K-RITH) Mycobacterial Genetics Course, University of California—Los Angeles Research Immersion Laboratory in Virology, Phage Hunters Integrating Research and Education (PHIRE) Program 2013; Complete genome sequences of 63 mycobacteriophages. Genome Announc 1:e00847-13 [View Article][PubMed]
    [Google Scholar]
  25. Hatfull G. F. 2015; Dark matter of the biosphere: the amazing world of bacteriophage diversity. J Virol 89:8107–8110 [View Article][PubMed]
    [Google Scholar]
  26. Hatfull G. F. Science Education Alliance Phage Hunters Advancing Genomics and Evolutionary Science Program, KwaZulu-Natal Research Institute for Tuberculosis and HIV Mycobacterial Genetics Course Students, Phage Hunters Integrating Research and Education Program 2012; Complete genome sequences of 138 mycobacteriophages. J Virol 86:2382–2384 [View Article][PubMed]
    [Google Scholar]
  27. Hatfull G. F., Jacobs-Sera D., Lawrence J. G., Pope W. H., Russell D. A., Ko C. C., Weber R. J., Patel M. C., Germane K. L. et al. 2010; Comparative genomic analysis of 60 Mycobacteriophage genomes: genome clustering, gene acquisition, and gene size. J Mol Biol 397:119–143 [View Article][PubMed]
    [Google Scholar]
  28. Henry M., O'Sullivan O., Sleator R. D., Coffey A., Ross R. P., McAuliffe O., O'Mahony J. M. 2010; In silico analysis of Ardmore, a novel mycobacteriophage isolated from soil. Gene 453:9–23 [View Article][PubMed]
    [Google Scholar]
  29. Hershberg R., Petrov D. A. 2010; Evidence that mutation is universally biased towards AT in bacteria. PLoS Genet 6:e1001115 [View Article][PubMed]
    [Google Scholar]
  30. Hildebrand F., Meyer A., Eyre-Walker A. 2010; Evidence of selection upon genomic GC-content in bacteria. PLoS Genet 6:e1001107 [View Article][PubMed]
    [Google Scholar]
  31. Hilterbrand A., Saelens J., Putonti C. 2012; CBDB: the codon bias database. BMC Bioinformatics 13:62 [View Article][PubMed]
    [Google Scholar]
  32. Huson D. H., Bryant D. 2006; Application of phylogenetic networks in evolutionary studies. Mol Biol Evol 23:254–267 [View Article][PubMed]
    [Google Scholar]
  33. Jacobs-Sera D., Marinelli L. J., Bowman C., Broussard G. W., Guerrero Bustamante C., Boyle M. M., Petrova Z. O., Dedrick R. M., Pope W. H. et al. 2012; On the nature of mycobacteriophage diversity and host preference. Virology 434:187–201 [View Article][PubMed]
    [Google Scholar]
  34. Kallimanis A., Karabika E., Mavromatis K., Lapidus A., Labutti K. M., Liolios K., Ivanova N., Goodwin L., Woyke T. et al. 2011; Complete genome sequence of Mycobacterium sp. strain (Spyr1) and reclassification to Mycobacterium gilvum Spyr1. Stand Genomic Sci 5:144–153 [View Article][PubMed]
    [Google Scholar]
  35. Kim B. J., Kim B. R., Hong S. H., Seok S. H., Kook Y. H., Kim B. J. 2013; Complete genome sequence of Mycobacterium massiliense clinical strain Asan 50594, belonging to the type II genotype. Genome Announc 1:e0042913 [View Article][PubMed]
    [Google Scholar]
  36. Kim B. J., Choi B. S., Lim J. S., Choi I. Y., Lee J. H., Chun J., Kook Y. H., Kim B. J. 2012; Complete genome sequence of Mycobacterium intracellulare strain ATCC 13950T . J Bacteriol 194:2750 [View Article][PubMed]
    [Google Scholar]
  37. Kudla G., Murray A. W., Tollervey D., Plotkin J. B. 2009; Coding-sequence determinants of gene expression in Escherichia coli . Science 324:255–258 [View Article][PubMed]
    [Google Scholar]
  38. Lawrence J. G., Hendrix R. W., Casjens S. 2001; Where are the pseudogenes in bacterial genomes?. Trends Microbiol 9:535–540 [View Article][PubMed]
    [Google Scholar]
  39. Li L., Bannantine J. P., Zhang Q., Amonsin A., May B. J., Alt D., Banerji N., Kanjilal S., Kapur V. 2005; The complete genome sequence of Mycobacterium avium subspecies paratuberculosis . Proc Natl Acad Sci U S A 102:12344–12349 [View Article][PubMed]
    [Google Scholar]
  40. Lowe T. M., Eddy S. R. 1997; tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Res 25:955–964 [View Article][PubMed]
    [Google Scholar]
  41. Lucks J. B., Nelson D. R., Kudla G. R., Plotkin J. B. 2008; Genome landscapes and bacteriophage codon usage. PLoS Comput Biol 4:e1000001 [View Article][PubMed]
    [Google Scholar]
  42. Michely S., Toulza E., Subirana L., John U., Cognat V., Maréchal-Drouard L., Grimsley N., Moreau H., Piganeau G. 2013; Evolution of codon usage in the smallest photosynthetic eukaryotes and their giant viruses. Genome Biol Evol 5:848–859 [View Article][PubMed]
    [Google Scholar]
  43. Mira A., Ochman H., Moran N. A. 2001; Deletional bias and the evolution of bacterial genomes. Trends Genet 17:589–596 [View Article][PubMed]
    [Google Scholar]
  44. Mitchell D. 2007; GC content and genome length in Chargaff compliant genomes. Biochem Biophys Res Commun 353:207–210 [View Article][PubMed]
    [Google Scholar]
  45. Musto H., Naya H., Zavala A., Romero H., Alvarez-Valín F., Bernardi G. 2006; Genomic GC level, optimal growth temperature, and genome size in prokaryotes. Biochem Biophys Res Commun 347:1–3 [View Article][PubMed]
    [Google Scholar]
  46. Parmley J. L., Hurst L. D. 2007; How do synonymous mutations affect fitness?. Bioessays 29:515–519 [View Article][PubMed]
    [Google Scholar]
  47. Pedulla M. L., Ford M. E., Houtz J. M., Karthikeyan T., Wadsworth C., Lewis J. A., Jacobs-Sera D., Falbo J., Gross J. et al. 2003; Origins of highly mosaic mycobacteriophage genomes. Cell 113:171–182 [View Article][PubMed]
    [Google Scholar]
  48. Plotkin J. B., Kudla G. 2011; Synonymous but not the same: the causes and consequences of codon bias. Nat Rev Genet 12:32–42 [View Article][PubMed]
    [Google Scholar]
  49. Pope W. H., Jacobs-Sera D., Russell D. A., Peebles C. L., Al-Atrache Z., Alcoser T. A., Alexander L. M., Alfano M. B., Alford S. T. et al. 2011; Expanding the diversity of mycobacteriophages: insights into genome architecture and evolution. PLoS One 6:E16329 [View Article][PubMed]
    [Google Scholar]
  50. Pope W. H., Jacobs-Sera D., Russell D. A., Rubin D. H., Kajee A., Msibi Z. N., Larsen M. H., Jacobs W. R., Lawrence J. G. et al. 2014; Genomics and proteomics of mycobacteriophage Patience, an accidental tourist in the Mycobacterium neighborhood. MBio 5:e02145 [View Article][PubMed]
    [Google Scholar]
  51. Pope W. H., Bowman C. A., Russell D. A., Jacobs-Sera D., Asai D. J., Cresawn S. G., Jacobs W. R., Hendrix R. W., Lawrence J. G. et al. 2015; Whole genome comparison of a large collection of mycobacteriophages reveals a continuum of phage genetic diversity. Elife 4:e06416e06416 [View Article][PubMed]
    [Google Scholar]
  52. Ran W., Kristensen D. M., Koonin E. V. 2014; Coupling between protein level selection and codon usage optimization in the evolution of bacteria and archaea. MBio 5:e00956-14 [View Article][PubMed]
    [Google Scholar]
  53. Rybniker J., Kramme S., Small P. L. 2006; Host range of 14 mycobacteriophages in Mycobacterium ulcerans and seven other mycobacteria including Mycobacterium tuberculosis – application for identification and susceptibility testing. J Med Microbiol 55:37–42 [View Article][PubMed]
    [Google Scholar]
  54. Sampson T., Broussard G. W., Marinelli L. J., Jacobs-Sera D., Ray M., Ko C. C., Russell D., Hendrix R. W., Hatfull G. F. 2009; Mycobacteriophages BPs, Angel and Halo: comparative genomics reveals a novel class of ultra-small mobile genetic elements. Microbiology 155:2962–2977 [View Article][PubMed]
    [Google Scholar]
  55. Schattner P., Brooks A. N., Lowe T. M. 2005; The tRNAscan-SE, snoscan and snoGPS web servers for the detection of tRNAs and snoRNAs. Nucleic Acids Res 33:W686–689 [View Article][PubMed]
    [Google Scholar]
  56. Sharp P. M., Li W. H. 1987; The codon adaptation Index–a measure of directional synonymous codon usage bias, and its potential applications. Nucleic Acids Res 15:1281–1295 [View Article][PubMed]
    [Google Scholar]
  57. Stinear T. P., Mve-Obiang A., Small P. L., Frigui W., Pryor M. J., Brosch R., Jenkin G. A., Johnson P. D., Davies J. K. et al. 2004; Giant plasmid-encoded polyketide synthases produce the macrolide toxin of Mycobacterium ulcerans . Proc Natl Acad Sci U S A 101:1345–1349 [View Article][PubMed]
    [Google Scholar]
  58. Stinear T. P., Seemann T., Harrison P. F., Jenkin G. A., Davies J. K., Johnson P. D., Abdellah Z., Arrowsmith C., Chillingworth T. et al. 2008; Insights from the complete genome sequence of Mycobacterium marinum on the evolution of Mycobacterium tuberculosis . Genome Res 18:729–741 [View Article][PubMed]
    [Google Scholar]
  59. Tamura K., Stecher G., Peterson D., Filipski A., Kumar S. 2013; mega6: Molecular Evolutionary Genetics Analysis version 6.0. Mol Biol Evol 30:2725–2729 [View Article][PubMed]
    [Google Scholar]
  60. Tortoli E. 2012; Phylogeny of the genus Mycobacterium: many doubts, few certainties. Infect Genet Evol 12:827–831 [View Article][PubMed]
    [Google Scholar]
  61. Tringe S. G., von Mering C., Kobayashi A., Salamov A. A., Chen K., Chang H. W., Podar M., Short J. M., Mathur E. J. et al. 2005; Comparative metagenomics of microbial communities. Science 308:554–557 [View Article][PubMed]
    [Google Scholar]
  62. Wan X. F., Xu D., Kleinhofs A., Zhou J. 2004; Quantitative relationship between synonymous codon usage bias and GC composition across unicellular genomes. BMC Evol Biol 4:19 [View Article][PubMed]
    [Google Scholar]
  63. Wan X.-F., Zhou J., Xu D. 2006; CodonO: a new informatics method for measuring synonymous codon usage bias within and across genomes. Int J Gen Syst 35:109–125 [View Article]
    [Google Scholar]
  64. Xia X., Yuen K. Y. 2005; Differential selection and mutation between dsDNA and ssDNA phages shape the evolution of their genomic AT percentage. BMC Genet 6:20 [View Article][PubMed]
    [Google Scholar]
  65. Alferez, G. I., Bryan, W. J., Byington, E. L., & other authors . NCBI GenBank http://www.ncbi.nlm.nih.gov/nuccore/JF704105 - GenBank Accession #: JF704105 2012
  66. Bambawale, V., Bieberich, J. C., Borowski, A. L., & other authors . NCBI GenBank http://www.ncbi.nlm.nih.gov/nuccore/JF704116 - GenBank Accession #: JF704116 2012
  67. Brosch, R., Gordon, S. V., Garnier, T., & other authors. Genome plasticity of BCG and impact on vaccine efficacy. Proc Natl Acad Sci USA 104, 5596-5601. GenBank Accession #: NC_008769 2007
  68. Cole, S. T., Brosch, R., Parkhill, J., & other authors. Deciphering the biology of Mycobacterium tuberculosis from the complete genome sequence. Nature 393, 537-544. GenBank Accession #: NC_000962 2001
  69. Cole, S. T., Eiglmeier, K., Parkhill, J., & other authors. Massive gene decay in the leprosy bacillus. Nature 409, 1007-1011. GenBank Accession #: NC_002677 2001
  70. Copeland, A., Lucas S., Lapidus, A., & other authors. NCBI GenBank http://www.ncbi.nlm.nih.gov/nuccore/FJ641182 - GenBank Accession #: FJ641182 2009
  71. Gallien, S., Perrodou, E., Carapito, C., & other authors. Ortho-proteogenomics: multiple proteomes investigation through orthology and a new MS-based protocol. Genome Res 19, 128-135. GenBank Accession #: NC_018289 2010
  72. Hatfull, G.F., Jacobs-Sera, D., Lawrence, J.G. & other authors. Comparative genomic analysis of 60 mycobacteriophage genomes: genome clustering, gene acquisition, and gene size. J Mol Biol 397, 119-143. - GenBank Accession #s: EU744252, EU744251, AY500152, AY129332, DQ398048, AY129334, EU816589, DQ398049, DQ398044, EU770221, AY129337, EU826471, DQ398053, EU826467, EU826469, EU826466, FJ168660, FJ168661, DQ398047, DQ398051, FJ168662, DQ398041, AY129331, EU816591, EU816588, EU816590, AY129330, FJ174690, DQ398045, FJ174692, DQ398050, FJ174693, AY129336, EU568876, DQ398042, FJ174691, EU770222, AY129339, FJ168659, AY129333, AY129338, AF068845, AY129335, EU203571, DQ398052 2010
  73. Hatfull, SEA-PHAGES, & other authors. Complete genome sequences of 138 mycobacteriophages. J Virol 86, 2382–2384. - GenBank Accession #s: JF704093, JN699015, JN243856, JF792674, JN243857, JN083852, JN408459, JF704107, JN698999, JF937092, JN049605, JF704097, JF937094, JN699019, JF957060, JN831654, JN699005, JF704110, JF704091, JN699017, JN638753, JN006064, JN699010, JN699009, JF704103, JN618996, JN699004, JN698991, JN699006, JN699003, JF704095, JN698992, JN699018, JN699011, JF704104, JN699007, JF704092, JN412588, JF704096, JN412592, JN699626, JN699627, JN699013, JN624850, JN699014, JF937107, JF937091, JN391441, JN412590, JF937096, JN382248, JN006062, JF937106, JN006061, JN698996, JF937093, JN859129, JN542517, JN398368, JF937098, JF937102, JN020142, JF704117, JN699012, JF704115, JN699002, JN412593, JN699001, JF937090, JN698997, JF937101, JF957059, JN201525, JF704106, JN643714, JN185608, JN831653, JN243855, JF704108, JF704113, JF744988, JN680858, JN699628, JF937105, KC576783, JN256079, JN624851, JN698993, JN412591, JF704112, JF704100, JN698995, JN698994,JN412589 2012
  74. Hatfull, SEA-PHAGES, & other authors. The complete genome sequences of 63 mycobacteriophages. Genome Announc 1, e00847-13. - GenBank Accession #s: JX042578, JQ684677, KC661275, JX015524, JX307704, JX411619, KC661279, JQ512844, KC748970, KC691257, JQ911768, KC748968, KC691255, KC748971, KC748969, KC661277, JX411620, KC661280, JQ809702, JX042579, KC691254, KC661276, KC900379, KC691256, KF024728 2013
  75. Henry, M., O'Sullivan, O., Sleator, R. D., & other authors. In silico analysis of Ardmore, a novel mycobacteriophage isolated from soil. Gene 453, 9-23. GenBank Accession #: GU060500 2010
  76. Jacobs-Sera, D., Zellars, M., Wells, D. & other authors. NCBI GenBank http://www.ncbi.nlm.nih.gov/nuccore/GU339467.1 GenBank Accession #: GU339467 2010
  77. Kallimanis, A., Karabika, E., Mavromatis, K., & other authors. Complete genome sequence of Mycobacterium sp. strain (Spyr1) and reclassification to Mycobacterium gilvum Spyr1. Stand Genomic Sci 5, 144-153. GenBank Accession #: NC_014814 2011
  78. Kim, B. J., Choi, B. S., Lim, J. S., & other authors. Complete genome sequence of Mycobacterium intracellulare strain ATCC 13950. J Bacteriol 194, 2750. GenBank Accession #: NC_016946 2012
  79. Kim, B. J., Kim, B. R., Hong, S.H., & other authors. Complete genome sequence of Mycobacterium massiliense clinical strain Asan 50594, belonging to the Type II genotype. Genome Announc, 1, e00429-13. GenBank Accession #: CP004374 2013
  80. Li, L., Bannantine, J., Zhang, Q., & other authors. The complete genome sequence of Mycobacterium avium subspecies paratuberculosis. Proc Nat Acad Sc USA 102, 12344-12349. GenBank Accession #: NC_002944 2005
  81. Pope, W. H., Jacobs-Sera, D., Russell, D. A. & other authors . Expanding the diversity of mycobacteriophages: insights into genome architecture and evolution. PLoS One 6, E16329. GenBank Accession #s: HM152765, GQ303263, GQ303260, GQ303262, GQ303265, GQ303261, HM152764, HM152767, HM152763, GQ303266 2011
  82. Pope, W.H., Bowman, C.A., Russell, D.A. & other authors. Whole genome comparison of a large collection of mycobacteriophages reveals a continuum of phage genetic diversity. eLife 4, e06416-e06416. - GenBank Accession #s: JN698998, JN153085, JF937099, JN699016, JX307705, JN020140, JN572689, JN408461, JF957058, JF704098, KC661281, KC661272, JF704101, JF704111, JF704114, JX307702, KC661271, JQ809701, JX307703, JF937104 2015
  83. Sampson, T., Broussard, G. W., Marinelli, L. J., & other authors. Mycobacteriophages BPs, Angel and Halo: comparative genomics reveals a novel class of ultra-small mobile genetic elements. Microbiology-SGM 155, 2962-2977. GenBank Accession #: FJ973624 2009
  84. Stinear, T. P., Mve-Obiang, A., Small, P. L., & other authors. Giant plasmid-encoded polyketide synthases produce the macrolide toxin of Mycobacterium ulcerans. Proc Natl Acad Sci USA 101, 1345-1349. GenBank Accession #:NC_005916 2004
  85. Stinear, T. P., Seemann, T., Harrison, P. F., & other authors. Insights from the complete genome sequence of Mycobacterium marinum on the evolution of Mycobacterium tuberculosis Genome Res 18, 729-741. GenBank Accession #: NC_010612 2008
http://instance.metastore.ingenta.com/content/journal/mgen/10.1099/mgen.0.000079
Loading
/content/journal/mgen/10.1099/mgen.0.000079
Loading

Data & Media loading...

Supplements

Supplementary File 1

WORD
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error