Whole genome comparison of a large collection of mycobacteriophages reveals a continuum of phage genetic diversity

eLife

Volumn 4, Issue , 2015, Pages

  Pope, Welkin H ^a   Bowman, Charles A ^a   Russell, Daniel A ^a   Jacobs Sera, Deborah ^a   Asai, David J ^b   Cresawn, Steven G ^c   Jacobs, William R ^d   Hendrix, Roger W ^a   Lawrence, Jeffrey G ^a   Hatfull, Graham F ^a  

^a UNIVERSITY OF PITTSBURGH   (United States)

^b HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^c JAMES MADISON UNIVERSITY   (United States)

^d ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID SEQUENCE; ARTICLE; CONTROLLED STUDY; GENETIC VARIABILITY; MOSAICISM; MYCOBACTERIOPHAGE; MYCOBACTERIUM SMEGMATIS; NONHUMAN; NUCLEOTIDE SEQUENCE; POPULATION STRUCTURE; CLASSIFICATION; COMPARATIVE STUDY; COOPERATION; ETHICS; GENE FLOW; GENETIC VARIATION; GENETICS; HIGH THROUGHPUT SEQUENCING; INFORMATION DISSEMINATION; MANPOWER; MEDICAL RESEARCH; PHYLOGENY; PHYLOGEOGRAPHY; VIROLOGY; VIRUS GENOME;

VIRUS DNA;

BIOMEDICAL RESEARCH; COOPERATIVE BEHAVIOR; DNA, VIRAL; GENE FLOW; GENETIC VARIATION; GENOME, VIRAL; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; INFORMATION DISSEMINATION; MOSAICISM; MYCOBACTERIOPHAGES; MYCOBACTERIUM SMEGMATIS; PHYLOGENY; PHYLOGEOGRAPHY;

EID: 85018215086     PISSN: None     EISSN: 2050084X     Source Type: Journal    
DOI: 10.7554/eLife.06416     Document Type: Article

References (48)

1. Brown KL, Sarkis GJ, Wadsworth C, Hatfull GF. 1997. Transcriptional silencing by the mycobacteriophage L5 repressor. The EMBO Journal 16:5914–5921. doi: 10.1093/emboj/16.19.5914.
2. Buckling A, Brockhurst M. 2012. Bacteria-virus coevolution. Advances in Experimental Medicine and Biology 751: 347–370. doi: 10.1007/978-1-4614-3567-9_16.
3. Cresawn SG, Bogel M, Day N, Jacobs-Sera D, Hendrix RW, Hatfull GF. 2011. Phamerator: a bioinformatic tool for comparative bacteriophage genomics. BMC Bioinformatics 12:395. doi: 10.1186/1471-2105-12-395.
4. Cresawn SG, Pope WH, Jacobs-Sera D, Bowman CA, Russell DA, Dedrick RA, Adair T, Anders KR, Ball S, Bollivar D, Breitenberger C, Burnett SH, Butela K, Byrnes D, Carzo S, Cornely KA, Cross T, Daniels RL, Dunbar D, Findley AM, Gissendanner CR, Golebiewska UP, Hartzog GA, Hatherill JR, Hughes LE, Jalloh CS, De Los Santos C, Ekanam K, Khambule SL, King RA, King-Smith C, Klyczek K, Krukonis GP, Laing C, Lapin JS, Lopez AJ, Mkhwanazi SM, Molloy SD, Moran D, Munsamy V, Pacey E, Plymale R, Poxleitner M, Reyna N, Schildbach JF, Stukey J, Taylor SE, Ware VC, Wellmann AL, Westholm D, Wodarski D, Zajko M, Zikalala TS, Hendrix RW, Hatfull GF. 2015. Comparative genomics of cluster O mycobacteriophages. PLOS ONE 10:e0118725. doi: 10.1371/journal.pone. 0118725.
5. Deng L, Ignacio-Espinoza JC, Gregory AC, Poulos BT, Weitz JS, Hugenholtz P, Sullivan MB. 2014. Viral tagging reveals discrete populations in Synechococcus viral genome sequence space. Nature 513:242–245. doi: 10.1038/nature13459.
6. Grose JH, Casjens SR. 2014. Understanding the enormous diversity of bacteriophages: the tailed phages that infect the bacterial family Enterobacteriaceae. Virology 468–470:421–443. doi: 10.1016/j.virol.2014.08.024.
7. Grose JH, Jensen GL, Burnett SH, Breakwell DP. 2014. Erratum: genomic comparison of 83 Bacillus phages reveals 12 clusters, 14 singletons and remarkable diversity. BMC Genomics 15:1184. doi: 10.1186/1471-2164-15-855.
8. Hambly E, Suttle CA. 2005. The viriosphere, diversity, and genetic exchange within phage communities. Current Opinion in Microbiology 8:444–450. doi: 10.1016/j.mib.2005.06.005.
9. Hatfull GF. 2010. Mycobacteriophages: genes and genomes. Annual Review of Microbiology 64:331–356. doi: 10.1146/annurev.micro.112408.134233.
10. Hatfull GF. 2012. The secret lives of mycobacteriophages. Advances in Virus Research 82:179–288. doi: 10.1016/B978-0-12-394621-8.00015-7.
11. Hatfull GF, Hendrix RW. 2011. Bacteriophages and their genomes. Current Opinions in Virology 1:298–303. doi: 10.1016/j.coviro.2011.06.009.
12. Hatfull GF, Jacobs-Sera D, Lawrence JG, Pope WH, Russell DA, Ko CC, Weber RJ, Patel MC, Germane KL, Edgar RH, Hoyte NN, Bowman CA, Tantoco AT, Paladin EC, Myers MS, Smith AL, Grace MS, Pham TT, O’Brien MB, Vogelsberger AM, Hryckowian AJ, Wynalek JL, Donis-Keller H, Bogel MW, Peebles CL, Cresawn SG, Hendrix RW. 2010. Comparative genomic analysis of 60 mycobacteriophage genomes: genome clustering, gene acquisition, and gene size. Journal of Molecular Biology 397:119–143. doi: 10.1016/j.jmb.2010.01.011.
13. Hatfull GF, Pedulla ML, Jacobs-Sera D, Cichon PM, Foley A, Ford ME, Gonda RM, Houtz JM, Hryckowian AJ, Kelchner VA, Namburi S, Pajcini KV, Popovich MG, Schleicher DT, Simanek BZ, Smith AL, Zdanowicz GM, Kumar V, Peebles CL, Jacobs WR Jr, Lawrence JG, Hendrix RW. 2006. Exploring the mycobacteriophage metaproteome: phage genomics as an educational platform. PLOS Genetics 2:e92. doi: 10.1371/journal.pgen.0020092.
14. Hatfull GF, 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 Announcements 1. doi: 10.1128/genomeA.00847-13.
15. Hauser M, Mayer CE, Soding J. 2013. kClust: fast and sensitive clustering of large protein sequence databases. BMC Bioinformatics 14:248. doi: 10.1186/1471-2105-14-248.
16. Hendrix RW. 2003. Bacteriophage genomics. Current Opinion in Microbiology 6:506–511. doi: 10.1016/j.mib. 2003.09.004.
17. Hendrix RW, Smith MC, Burns RN, Ford ME, Hatfull GF. 1999. Evolutionary relationships among diverse bacteriophages and prophages: all the world’s a phage. Proceedings of the National Academy of Sciences of USA 96:2192–2197. doi: 10.1073/pnas.96.5.2192.
18. Hoskisson PA, Sumby P, Smith MC. 2015. The phage growth limitation system in Streptomyces coelicolor A(3)2 is a toxin/antitoxin system, comprising enzymes with DNA methyltransferase, protein kinase and ATPase activity. Virology 477:100–109. doi: 10.1016/j.virol.2014.12.036.
19. Hunter AB, Laursen SL, Seymour E. 2007. Becoming a scientist: the role of undergraduate research in students’ cognitive, personal, and professional development. Science Education 91:36–74. doi: 10.1002/sce.20173.
20. Huson DH. 1998. SplitsTree: analyzing and visualizing evolutionary data. Bioinformatics 14:68–73. doi: 10.1093/bioinformatics/14.1.68.
21. Huson DH, Bryant D. 2006. Application of phylogenetic networks in evolutionary studies. Molecular Biology and Evolution 23:254–267. doi: 10.1093/molbev/msj030.
22. Ignacio-Espinoza JC, Solonenko SA, Sullivan MB. 2013. The global virome: not as big as we thought? Current Opinion in Virology 3:566–571. doi: 10.1016/j.coviro.2013.07.004.
23. Jacobs-Sera D, Marinelli LJ, Bowman C, Broussard GW, Guerrero Bustamante C, Boyle MM, Petrova ZO, Dedrick RM, Pope WH, Science Education Alliance Phage Hunters Advancing Genomics And Evolutionary Science Sea-Phages Program Modlin RL, Hendrix RW, Hatfull GF. 2012. On the nature of mycobacteriophage diversity and host preference. Virology 434:187–201. doi: 10.1016/j.virol.2012.09.026.
24. Jordan TC, Burnett SH, Carson S, Caruso SM, Clase K, DeJong RJ, Dennehy JJ, Denver DR, Dunbar D, Elgin SC, Findley AM, Gissendanner CR, Golebiewska UP, Guild N, Hartzog GA, Grillo WH, Hollowell GP, Hughes LE, Johnson A, King RA, Lewis LO, Li W, Rosenzweig F, Rubin MR, Saha MS, Sandoz J, Shaffer CD, Taylor B, Temple L, Vazquez E, Ware VC, Barker LP, Bradley KW, Jacobs-Sera D, Pope WH, Russell DA, Cresawn SG, Lopatto D, Bailey CP, Hatfull GF. 2014. A broadly implementable research course in phage discovery and genomics for first-year undergraduate students. mBio 5:e01051–01013. doi: 10.1128/mBio.01051-13.
25. Juhala RJ, Ford ME, Duda RL, Youlton A, Hatfull GF, Hendrix RW. 2000. Genomic sequences of bacteriophages HK97 and HK022: pervasive genetic mosaicism in the lambdoid bacteriophages. Journal of Molecular Biology 299:27–51. doi: 10.1006/jmbi.2000.3729.
26. Kropinski AM, Sulakvelidze A, Konczy P, Poppe C. 2007. Salmonella phages and prophages–genomics and practical aspects. Methods in Molecular Biology 394:133–175. doi: 10.1007/978-1-59745-512-1_9.
27. Krumsiek J, Arnold R, Rattei T. 2007. Gepard: a rapid and sensitive tool for creating dotplots on genome scale. Bioinformatics 23:1026–1028. doi: 10.1093/bioinformatics/btm039.
28. Krupovic M, Bamford DH. 2010. Order to the viral universe. Journal of Virology 84:12476–12479. doi: 10.1128/JVI.01489-10.
29. Kwan T, Liu J, Dubow M, Gros P, Pelletier J. 2006. Comparative genomic analysis of 18 Pseudomonas aeruginosa bacteriophages. Journal of Bacteriology 188:1184–1187. doi: 10.1128/JB.188.3.1184-1187.2006.
30. Kwan T, Liu J, DuBow M, Gros P, Pelletier J. 2005. The complete genomes and proteomes of 27 Staphylococcus aureus bacteriophages. Proceedings of the National Academy of Sciences of USA 102:5174–5179. doi: 10.1073/pnas.0501140102.
31. Lassmann T, Sonnhammer EL. 2005. Kalign–an accurate and fast multiple sequence alignment algorithm. BMC Bioinformatics 6:298. doi: 10.1186/1471-2105-6-298.
32. Lawrence JG, Hatfull GF, Hendrix RW. 2002. Imbroglios of viral taxonomy: genetic exchange and failings of phenetic approaches. Journal of Bacteriology 184:4891–4905. doi: 10.1128/JB.184.17.4891-4905.2002.
33. Lee JH, Shin H, Ryu S. 2014. Characterization and comparative genomic analysis of bacteriophages infecting members of the Bacillus cereus group. Archives of Virology 159:871–884. doi: 10.1007/s00705-013-1920-3.
34. Lima-Mendez G, Toussaint A, Leplae R. 2007. Analysis of the phage sequence space: the benefit of structured information. Virology 365:241–249. doi: 10.1016/j.virol.2007.03.047.
35. Marinelli LJ, Fitz-Gibbon S, Hayes C, Bowman C, Inkeles M, Loncaric A, Russell DA, Jacobs-Sera D, Cokus S, Pellegrini M, Kim J, Miller JF, Hatfull GF, Modlin RL. 2012. Propionibacterium acnes bacteriophages display limited genetic diversity and broad killing activity against bacterial skin isolates. mBio 3. doi: 10.1128/mBio. 00279-12.
36. Mokili JL, Rohwer F, Dutilh BE. 2012. Metagenomics and future perspectives in virus discovery. Current Opinion in Virology 2:63–77. doi: 10.1016/j.coviro.2011.12.004.
37. PCAST, PsCoSaT. 2012. Report to the president. Engage to excel: producing one million additional college graduates with degrees in science, technology, engineering, and mathematics. Executive Office of the President. Washington, DC.
38. Pedulla ML, Ford ME, Houtz JM, Karthikeyan T, Wadsworth C, Lewis JA, Jacobs-Sera D, Falbo J, Gross J, Pannunzio NR, Brucker W, Kumar V, Kandasamy J, Keenan L, Bardarov S, Kriakov J, Lawrence JG, Jacobs WR, Hendrix RW, Hatfull GF. 2003. Origins of highly mosaic mycobacteriophage genomes. Cell 113:171–182. doi: 10. 1016/S0092-8674(03)00233-2.
39. Petrov VM, Ratnayaka S, Nolan JM, Miller ES, Karam JD. 2010. Genomes of the T4-related bacteriophages as windows on microbial genome evolution. Virology Journal 7:292. doi: 10.1186/1743-422X-7-292.
40. Pope WH, Anders KR, Baird M, Bowman CA, Boyle MM, Broussard GW, Chow T, Clase KL, Cooper S, Cornely KA, Dejong RJ, Delesalle VA, Deng L, Dunbar D, Edgington NP, Ferreira CM, Weston Hafer K, Hartzog GA, Hatherill JR, Hughes LE, Ipapo K, Krukonis GP, Meier CG, Monti DL, Olm MR, Page ST, Peebles CL, Rinehart CA, Rubin MR, Russell DA, Sanders ER, Schoer M, Shaffer CD, Wherley J, Vazquez E, Yuan H, Zhang D, Cresawn SG, Jacobs-Sera D, Hendrix RW, Hatfull GF. 2014a. Cluster M mycobacteriophages Bongo, PegLeg, and Rey with unusually large repertoires of tRNA isotypes. Journal of Virology 88:2461–2480. doi: 10.1128/JVI.03363-13.
41. Pope WH, Ferreira CM, Jacobs-Sera D, Benjamin RC, Davis AJ, DeJong RJ, Elgin SCR, Guilfoile FR, Forsyth MH, Harris AD, Harvey SE, Hughes LE, Hynes PM, Jackson AS, Jalal MD, MacMurray EA, Manley CM, McDonough MJ, Mosier JL, Osterbann LJ, Rabinowitz HS, Rhyan CN, Russell DA, Saha MS, Shaffer CD, Simon SE, Sims EF, Tovar IG, Weisser EG, Wertz JT, Weston-Hafer KA, Williamson KE, Zhang B, Cresawn SG, Jain P, Piuri M, Jacobs WR Jr, Hendrix RW, Hatfull GF. 2011a. Cluster K mycobacteriophages: insights into the evolutionary origins of mycobacteriophage TM4. PLOS ONE 6:e26750. doi: 10.1371/journal.pone.0026750.
42. Pope WH, Jacobs-Sera D, Best AA, Broussard GW, Connerly PL, Dedrick RM, Kremer TA, Offner S, Ogiefo AH, Pizzorno MC, Rockenbach K, Russell DA, Stowe EL, Stukey J, Thibault SA, Conway JF, Hendrix RW, Hatfull GF. 2013. Cluster J mycobacteriophages: intron splicing in capsid and tail genes. PLOS ONE 8:e69273. doi: 10.1371/journal.pone.0069273.
43. Pope WH, Jacobs-Sera D, Russell DA, Peebles CL, Al-Atrache Z, Alcoser TA, Alexander LM, Alfano MB, Alford ST, Amy NE, Anderson MD, Anderson AG, Ang AAS, Ares M Jr, Barber AJ, Barker LP, Barrett JM, Barshop WD, Bauerle CM, Bayles IM, Belfield KL, Best AA, Borjon A Jr, Bowman CA, Boyer CA, Bradley KW, Bradley VA, Broadway LN, Budwal K, Busby KN, Campbell IW, Campbell AM, Carey A, Caruso SM, Chew RD, Cockburn CL, Cohen LB, Corajod JM, Cresawn SG, Davis KR, Deng L, Denver DR, Dixon BR, Ekram S, Elgin SCR, Engelsen AE, English BEV, Erb ML, Estrada C, Filliger LZ, Findley AM, Forbes L, Forsyth MH, Fox TM, Fritz MJ, Garcia R, George ZD, Georges AE, Gissendanner CR, Goff S, Goldstein R, Gordon KC, Green RD, Guerra SL, Guiney-Olsen KR, Guiza BG, Haghighat L, Hagopian GV, Harmon CJ, Harmson JS, Hartzog GA, Harvey SE, He S, He KJ, Healy KE, Higinbotham ER, Hildebrandt EN, Ho JH, Hogan GM, Hohenstein VG, Holz NA, Huang VJ, Hufford EL, Hynes PM, Jackson AS, Jansen EC, Jarvik J, Jasinto PG, Jordan TC, Kasza T, Katelyn MA, Kelsey JS, Kerrigan LA, Khaw D, Kim J, Knutter JZ, Ko CC, Larkin GV, Laroche JR, Latif A, Leuba KD, Leuba SI, Lewis LO, Loesser-Casey KE, Long CA, Lopez AJ, Lowery N, Lu TQ, Mac V, Masters IR, McCloud JJ, McDonough MJ, Medenbach AJ, Menon A, Miller R, Morgan BK, Ng PC, Nguyen E, Nguyen KT, Nguyen ET, Nicholson KM, Parnell LA, Peirce CE, Perz AM, Peterson LJ, Pferdehirt RE, Philip SV, Pogliano K, Pogliano J, Polley T, Puopolo EJ, Rabinowitz HS, Resiss MJ, Rhyan CN, Robinson YM, Rodriguez LL, Rose AC, Rubin JD, Ruby JA, Saha MS, Sandoz JW, Savitskaya J, Schipper DJ, Schnitzler CE, Schott AR, Segal JB, Shaffer CD, Sheldon KE, Shepard EM, Shepardson JW, Shroff MK, Simmons JM, Simms EF, Simpson BM, Sinclair KM, Sjoholm RL, Slette IJ, Spaulding BC, Straub CL, Stukey J, Sughrue T, Tang TY, Tatyana LM, Taylor SB, Taylor BJ, Temple LM, Thompson JV, Tokarz MP, Trapani SE, Troum AP, Tsay J, Tubbs AT, Walton JM, Wang DH, Wang H, Warner JR, Weisser EG, Wendler SC, Weston-Hafer KA, Whelan HM, Williamson KE, Willis AN, Wirtshafter HS, Wong TW, Wu P, Yang YJ, Yee BC, Zaidins DA, Zhang B, Zúniga MY, Hendrix RW, Hatfull GF. 2011b. Expanding the diversity of mycobacteriophages: insights into genome architecture and evolution. PLOS ONE 6:e16329. doi: 10.1371/journal.pone.0016329.
44. Pope WH, Jacobs-Sera D, Russell DA, Rubin DH, Kajee A, Msibi ZN, Larsen MH, Jacobs WR Jr, Lawrence JG, Hendrix RW, Hatfull GF. 2014b. Genomics and proteomics of mycobacteriophage patience, an accidental tourist in the mycobacterium neighborhood. mBio 5:e02145. doi: 10.1128/mBio.02145-14.
45. Remmert M, Biegert A, Hauser A, Soding J. 2012. HHblits: lightning-fast iterative protein sequence searching by HMM-HMM alignment. Nature Methods 9:173–175. doi: 10.1038/nmeth.1818.
46. Rodriguez-Brito B, Li L, Wegley L, Furlan M, Angly F, Breitbart M, Buchanan J, Desnues C, Dinsdale E, Edwards R, Felts B, Haynes M, Liu H, Lipson D, Mahaffy J, Martin-Cuadrado AB, Mira A, Nulton J, Pasic L, Rayhawk S, Rodriguez-Mueller J, Rodriguez-Valera F, Salamon P, Srinagesh S, Thingstad TF, Tran T, Thurber RV, Willner D, Youle M, Rohwer F. 2010. Viral and microbial community dynamics in four aquatic environments. The ISME Journal 4:739–751. doi: 10.1038/ismej.2010.1.
47. Rohwer F. 2003. Global phage diversity. Cell 113:141. doi: 10.1016/S0092-8674(03)00276-9.
48. Suttle CA. 2007. Marine viruses–major players in the global ecosystem. Nature Reviews Microbiology 5:801–812. doi: 10.1038/nrmicro1750.