The genome and structural proteome of an ocean siphovirus: A new window into the cyanobacterial 'mobilome'

Environmental Microbiology

Volumn 11, Issue 11, 2009, Pages 2935-2951

  Sullivan, Matthew B ^a,c   Krastins, Bryan ^b   Hughes, Jennifer L ^c   Kelly, Libusha ^a   Chase, Michael ^b   Sarracino, David ^b   Chisholm, Sallie W ^a  

^a Massachusetts Institute of Technology Cambridge   (United States)

^b Harvard Partners   (United States)

^c University of Arizona   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEOME; SEA WATER; VIRUS DNA; VIRUS PROTEIN;

ARTICLE; ATLANTIC OCEAN; BACTERIOPHAGE; CHEMISTRY; DNA SEQUENCE; GENETICS; INTERSPERSED REPEAT; MICROBIOLOGY; MOLECULAR GENETICS; PHYLOGENY; PROCHLOROCOCCUS; SEQUENCE HOMOLOGY; SYNTENY; VIROLOGY; VIRUS GENOME;

ATLANTIC OCEAN; BACTERIOPHAGES; DNA, VIRAL; GENOME, VIRAL; INTERSPERSED REPETITIVE SEQUENCES; MOLECULAR SEQUENCE DATA; PHYLOGENY; PROCHLOROCOCCUS; PROTEOME; SEAWATER; SEQUENCE ANALYSIS, DNA; SEQUENCE HOMOLOGY, AMINO ACID; SEQUENCE HOMOLOGY, NUCLEIC ACID; SIPHOVIRIDAE; SYNTENY; VIRAL STRUCTURAL PROTEINS;

CYANOBACTERIA; MIRIDAE; PODOCARPUS LATIFOLIUS; PROCHLOROCOCCUS; SYNECHOCOCCUS;

EID: 70350464284     PISSN: 14622912     EISSN: 14622920     Source Type: Journal    
DOI: 10.1111/j.1462-2920.2009.02081.x     Document Type: Article

References (94)

1. Baba, T., Takeuchi, F., Kuroda, M., Yuzawa, H., Aoki, K., Oguchi, A., et al. (2002) Genome and virulence determinants of high virulence community-acquired MRSA. Lancet 359 : 1819 1827.
2. Banks, D.J., Beres, S.B. Musser, J.M. (2002) The fundamental contribution of phages to GAS evolution, genome diversification and strain emergence. Trends Microbiol 10 : 515 521.
3. Barre, F.X. Sherratt, D.J. (2002) Xer site-specific recombination: promoting chromosome segregation. In Mobile DNA II. Craig, N.L., Craigie, R., Gellert, M. Lambowitz, A.M. (eds). Washington DC, USA : American Society for Microbiology Press, pp. 149 161.
4. Bartosik, D., Putyrski, M., Dziewit, L., Malewska, E., Szymanik, M., Jagiello, E., et al. (2008) Transposable modules generated by a single copy of insertion sequence ISPme1 and their influence on structure and evolution of natural plasmids of Paracoccus methylutens DM12. J Bacteriol 190 : 3306 3313.
5. Beres, S.B., Sylva, G.L., Barbian, K.D., Lei, B., Hoff, J.S., Mammarella, N.D., et al. (2002) Genome sequence of a serotype M3 strain of group A Streptococcus: phage-encoded toxins, the high-virulence phenotype, and clone emergence. Proc Natl Acad Sci USA 99 : 10078 10083.
6. Berg, D.E. Howe, M.M. (1989). Mobile DNA. Washington DC, USA : American Society for Microbiology Press.
7. Boyd, E.F., Davis, B.M. Hochhut, B. (2001) Bacteriophage-bacteriophage interactions in the evolution of pathogenic bacteria. Trends Microbiol 9 : 137 144.
8. Bragg, J.G. Chisholm, S.W. (2008) Modelling the fitness consequences of a cyanophage-encoded photosynthesis gene. PLoS One 3 : 3550.
9. Breitbart, M., Salamon, P., Andresen, B., Mahaffy, J.M., Segall, A.M., Mead, D., et al 2002) Genomic analysis of uncultured marine viral communities. Proc Natl Acad Sci USA 99 : 14250 14255.
10. Breitbart, M., Thompson, L.T., Suttle, C.A. Sullivan, M.B. (2007) Exploring the vast diversity of marine viruses. Oceanography 20 : 135 139.
11. Brussow, H. Desiere, F. (2001) Comparative phage genomics and the evolution of Siphoviridae: insights from dairy phages. Mol Microbiol 39 : 213 222.
12. Bushman, F. (2002) Lateral DNA Transfer: Mechanisms and Consequences. Cold Spring Harbor, NY, USA : Cold Spring Harbor University Press.
13. Calendar, R. (1988) The Bacteriophages. New York, USA : Plenum.
14. Campbell, A. (2003) Prophage insertion sites. Res Microbiol 154 : 277 282.
15. Canchaya, C., Proux, C., Fournous, G., Bruttin, A. Brussow, H. (2003) Prophage genomics. Microbiol Mol Biol Rev 67 : 238 276.
16. Casjens, S. (2003) Prophages and bacterial genomics: what have we learned so far? Mol Microbiol 49 : 277 300.
17. Casjens, S., Gilcrease, E.B., Winn-Stapley, D.A., Schicklmaier, P., Schmieger, H., Pedulla, M.L., et al. (2005) The generalized transducing Salmonella bacteriophage ES18: complete genome sequence and DNA packaging strategy. J Bacteriol 187 : 1091 1104.
18. Chen, F. Lu, J. (2002) Genomic sequence and evolution of marine cyanophage P60: a new insight on lytic and lysogenic phages. Appl Environ Microbiol 68 : 2589 2594.
19. Chen, F., Wang, K., Stewart, J. Belas, R. (2006) Induction of multiple prophages from a marine bacterium: a genomic approach. Appl Environ Microbiol 72 : 4995 5001.
20. Chibani-Chennoufi, S., Bruttin, A., Dillmann, M.L. Brussow, H. (2004) Phage-host interaction: an ecological perspective. J Bacteriol 186 : 3677 3686.
21. Clokie, M.R.J., Shan, J., Bailey, S., Jia, Y. Krisch, H.M. (2006) Transcription of a 'photosynthetic' T4-type phage during infection of a marine cyanobacterium. Environ Microbiol 8 : 827 835.
22. Coleman, M.L., Sullivan, M.B., Martiny, A.C., Steglich, C., Barry, K., Delong, E.F. Chisholm, S.W. (2006) Genomic islands and the ecology and evolution of Prochlorococcus. Science 311 : 1768 1770.
23. Dufresne, A., Salanoubat, M., Partensky, F., Artiguenave, F., Axmann, I.M., Barbe, V., et al. (2003) Genome sequence of the cyanobacterium Prochlorococcus marinus SS120, a nearly minimal oxyphototrophic genome. Proc Natl Acad Sci USA 100 : 10020 10025.
24. Dufresne, A., Ostrowski, M., Scanlan, D.J., Garczarek, L., Mazard, S., Palenik, B.P., et al. (2008) Unraveling the genomic mosaic of a ubiquitous genus of marine cyanobacteria. Genome Biol 9 : R90.
25. Edwards, R.A. Rohwer, F. (2005) Viral metagenomics. Nat Rev Microbiol 3 : 504 510.
26. Elias, J.E. Gygi, S.P. (2007) Target-decoy search strategy for increased confidence in large-scale protein identifications by mass spectrometry. Nat Methods 4 : 207 214.
27. Fuhrman, J.A. (2000) Impact of viruses on bacterial processes. In Microbial Ecology of the Oceans. Kirchman, D.L. (ed.). New York, USA : Wiley-Liss, pp. 327 350.
28. Hellweger, F.L. (2009) Carrying photosynthesis genes increases ecological fitness of cyanophage in silico. Environ Microbiol 11 : 1386 1394.
29. Hendrix, R.W., Smith, M.C., Burns, R.N., Ford, M.E. Hatfull, G.F. (1999) Evolutionary relationships among diverse bacteriophages and prophages: all the world's a phage. Proc Natl Acad Sci USA 96 : 2192 2197.
30. Huber, K.E. Waldor, M.K. (2002) Filamentous phage integration requires the host recombinases XerC and XerD. Nature 417 : 656 659.
31. Johnson, Z.I., Zinser, E.R., Coe, A., McNulty, N.P., Woodward, E.M. Chisholm, S.W. (2006) Niche partitioning among Prochlorococcus ecotypes along ocean-scale environmental gradients. Science 311 : 1737 1740.
32. Juhala, R.J., Ford, M.E., Duda, R.L., Youlton, A., Hatfull, G.F. Hendrix, R.W. (2000) Genomic sequences of bacteriophages HK97 and HK022: pervasive genetic mosaicism in the lambdoid bacteriophages. J Mol Biol 299 : 27 51.
33. Kettler, G.C., Martiny, A.C., Huang, K., Zucker, J., Coleman, M.L., Rodrigue, S., et al. (2007) Patterns and implications of gene gain and loss in the evolution of Prochlorococcus. PLoS Genet 3 : e231.
34. Kingsford, C.L., Ayanbule, K. Salzberg, S.L. (2007) Rapid, accurate, computational discovery of Rho-independent transcription terminators illuminates their relationship to DNA uptake. Genome Biol 8 : R22.
35. Lawrence, J.G., Hatfull, G.F. Hendrix, R.W. (2002) Imbroglios of viral taxonomy: genetic exchange and failings of phenetic approaches. J Bacteriol 184 : 4891 4905.
36. Leplae, R., Hebrant, A., Wodak, S.J. Toussaint, A. (2004) ACLAME: a CLAssification of Mobile genetic Elements. Nucleic Acids Res 32 : D45 D49.
37. Lindell, D., Sullivan, M.B., Johnson, Z.I., Tolonen, A.C., Rohwer, F. Chisholm, S.W. (2004) Transfer of photosynthesis genes to and from Prochlorococcus viruses. Proc Natl Acad Sci USA 101 : 11013 11018.
38. Lindell, D., Jaffe, J.D., Johnson, Z.I., Church, G.M. Chisholm, S.W. (2005) Photosynthesis genes in marine viruses yield proteins during host infection. Nature 438 : 86 89.
39. Lindell, D., Jaffe, J.D., Coleman, M.L., Futschik, M.E., Axmann, I.M., Rector, T., et al. (2007) Genome-wide expression dynamics of a marine virus and host reveal features of co-evolution. Nature 449 : 83 86.
40. Lohr, J.E., Chen, F. Hill, R.T. (2005) Genomic analysis of bacteriophage PhiJL001: insights into its interaction with a sponge-associated alpha-proteobacterium. Appl Environ Microbiol 71 : 1598 1609.
41. Lonetto, M., Gribskov, M. Gross, C.A. (1992) The sigma-70 family: sequence conservation and evolutionary relationships. J Bacteriol 174 : 3843 3849.
42. Lu, J., Chen, F. Hodson, R.E. (2001) Distribution, isolation, host specificity, and diversity of cyanophages infecting marine Synechococcus spp. in river estuaries. Appl Environ Microbiol 67 : 3285 3290.
43. McDaniel, L., Houchin, L.A., Williamson, S.J. Paul, J.H. (2002) Lysogeny in marine Synechococcus. Nature 415 : 496.
44. Mahillon, J. Chandler, M. (1998) Insertion sequences. Microbiol Mol Biol Rev 62 : 725 774.
45. Mann, N.H., Cook, A., Millard, A., Bailey, S. Clokie, M. (2003) Bacterial photosynthesis genes in a virus. Nature 424 : 741.
46. Mann, N.H., Clokie, M.R., Millard, A., Cook, A., Wilson, W.H., Wheatley, P.J., et al. (2005) The genome of S-PM2, a 'photosynthetic' T4-type bacteriophage that infects marine Synechococcus. J Bacteriol 187 : 3188 3200.
47. Marston, M.F. Sallee, J.L. (2003) Genetic diversity and temporal variation in the cyanophage community infecting marine Synechococcus species in Rhode Island's coastal waters. Appl Environ Microbiol 69 : 4639 4647.
48. Martiny, A.C., Coleman, M.L. Chisholm, S.W. (2006) Phosphate acquisition genes in Prochlorococcus ecotypes: evidence for genome-wide adaptation. Proc Natl Acad Sci USA 103 : 12552 12557.
49. Miao, E.A. Miller, S.I. (1999) Bacteriophages in the evolution of pathogen-host interactions. Proc Natl Acad Sci USA 96 : 9452 9454.
50. Millard, A., Clokie, M.R., Shub, D.A. Mann, N.H. (2004) Genetic organization of the psbAD region in phages infecting marine Synechococcus strains. Proc Natl Acad Sci USA 101 : 11007 11012.
51. Miller, E.S., Heidelberg, J.F., Eisen, J.A., Nelson, W.C., Durkin, A.S., Ciecko, A., et al. (2003) Complete genome sequence of the broad-host-range vibriophage KVP40: comparative genomics of a T4-related bacteriophage. J Bacteriol 185 : 5220 5233.
52. Moran, N.A. Plague, G.R. (2004) Genomic changes following host restriction in bacteria. Curr Opin Genet Dev 14 : 627 633.
53. Muhling, M., Fuller, N.J., Millard, A., Somerfield, P.J., Marie, D., Wilson, W.H., et al. (2005) Genetic diversity of marine Synechococcus and co-occurring cyanophage communities: evidence for viral control of phytoplankton. Environ Microbiol 7 : 499 508.
54. Nojiri, H., Shintani, M. Omori, T. (2004) Divergence of mobile genetic elements involved in the distribution of xenobiotic-catabolic capacity. Appl Microbiol Biotechnol 64 : 154 174.
55. Nolan, J.M., Petrov, V., Bertrand, C., Krisch, H.M. Karam, J.D. (2006) Genetic diversity among five T4-like bacteriophages. Virol J 3 : 30.
56. Oakey, H.J., Cullen, B.R. Owens, L. (2002) The complete nucleotide sequence of the Vibrio harveyi bacteriophage VHML. J Appl Microbiol 93 : 1089 1098.
57. Ortmann, A.C., Lawrence, J.E. Suttle, C.A. (2002) Lysogeny and lytic viral production during a bloom of the cyanobacterium Synechococcus spp. Microb Ecol 43 : 225 231.
58. Palenik, B., Brahamsha, B., McCarren, J., Waterbury, J., Allen, E., Webb, E.A., et al. (2003) The genome of a motile marine Synechococcus. Nature 424 : 1037 1041.
59. Palenik, B., Ren, Q., Dupont, C.L., Myers, G.S., Heidelberg, J.F., Badger, J.H., et al. (2006) Genome sequence of Synechococcus CC9311: insights into adaptation to a coastal environment. Proc Natl Acad Sci USA 103 : 13555 13559.
60. Partensky, F., Hess, W.R. Vaulot, D. (1999) Prochlorococcus, a marine photosynthetic prokaryote of global significance. Microbiol Mol Biol Rev 63 : 106 127.
61. Pedulla, M.L., Ford, M.E., Houtz, J.M., Karthikeyan, T., Wadsworth, C., Lewis, J.A., et al. (2003) Origins of highly mosaic mycobacteriophage genomes. Cell 113 : 171 182.
62. Pei, J. Grishin, N.V. (2007) PROMALS: towards accurate multiple sequence alignments of distantly related proteins. Bioinformatics 23 : 802 808.
63. Pei, J., Kim, B.H., Tang, M. Grishin, N.V. (2007) PROMALS web server for accurate multiple protein sequence alignments. Nucleic Acids Res 35 : W649 W652.
64. Plague, G.R., Dunbar, H.E., Tran, P.L. Moran, N.A. (2008) Extensive proliferation of transposable elements in heritable bacterial symbionts. J Bacteriol 190 : 777 779.
65. Poirel, L., Lartigue, M.F., Decousser, J.W. Nordmann, P. (2005) ISEcp1B-mediated transposition of blaCTX-M in Escherichia coli. Antimicrob Agents Chemother 49 : 447 450.
66. Pope, W.H.W.P., Chang, J., Pedulla, M.L., Ford, M.E., Houtz, J.M., Jiang, W., et al. (2007) Genome sequence, structural proteins, and capsid organization of the cyanophage Syn5: a 'horned' bacteriophage of marine Synechococcus. J Mol Biol 368 : 966 981.
67. Proux, C., van Sinderen, D., Suarez, J., Garcia, P., Ladero, V., Fitzgerald, G.F., et al. (2002) The dilemma of phage taxonomy illustrated by comparative genomics of Sfi21-like Siphoviridae in lactic acid bacteria. J Bacteriol 184 : 6026 6036.
68. van Regenmortel, M.H.V., Fauquet, C.M., Bishop, D.H.L., Carstens, E.B., Estes, M.K., Lemon, S.M., et al 2000) Virus Taxonomy: The Classification and Nomenclature of Viruses. San Diego, USA : Academic Press.
69. Rice, P., Longden, I. Bleasby, A. (2000) EMBOSS: the European Molecular Biology Open Software Suite. Trends Genet 16 : 276 277.
70. Rocap, G., Larimer, F.W., Lamerdin, J., Malfatti, S., Chain, P., Ahlgren, N.A., et al. (2003) Genome divergence in two Prochlorococcus ecotypes reflects oceanic niche differentiation. Nature 424 : 1042 1047.
71. Rohwer, F., Segall, A., Steward, G., Seguritan, V., Breitbart, M., Wolven, F. Azam, F. (2000) The complete genomic sequence of the marine phage Roseophage SIO1 shares homology with nonmarine phages. Limnol Oceanogr 45 : 408 418.
72. Rusch, D.B., Halpern, A.L., Sutton, G., Heidelberg, K.B., Williamson, S., Yooseph, S., et al 2007) The Sorcerer II Global Ocean Sampling Expedition: Northwest Atlantic through Eastern Tropical Pacific. PLoS Biol 5 : e77.
73. Rutherford, K., Parkhill, J., Crook, J., Horsnell, T., Rice, P., Rajandream, M.A. Barrell, B. (2000) Artemis: sequence visualization and annotation. Bioinformatics 16 : 944 945.
74. Schneider, D. Lenski, R.E. (2004) Dynamics of insertion sequence elements during experimental evolution of bacteria. Res Microbiol 155 : 319 327.
75. Simpson, A.J., Reinach, F.C., Arruda, P., Abreu, F.A., Acencio, M., Alvarenga, R., et al. (2000) The genome sequence of the plant pathogen Xylella fastidiosa. The Xylella fastidiosa Consortium of the Organization for Nucleotide Sequencing and Analysis. Nature 406 : 151 157.
76. Smoot, J.C., Barbian, K.D., Van Gompel, J.J., Smoot, L.M., Chaussee, M.S., Sylva, G.L., et al. (2002) Genome sequence and comparative microarray analysis of serotype M18 group A Streptococcus strains associated with acute rheumatic fever outbreaks. Proc Natl Acad Sci USA 99 : 4668 4673.
77. Smoot, L.M., Smoot, J.C., Graham, M.R., Somerville, G.A., Sturdevant, D.E., Migliaccio, C.A., et al. (2001) Global differential gene expression in response to growth temperature alteration in group A Streptococcus. Proc Natl Acad Sci USA 98 : 10416 10421.
78. Stamatakis, A. (2006) RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22 : 2688 2690.
79. Stamatakis, A., Hoover, P. Rougemont, J. (2008) A rapid bootstrap algorithm for the RAxML web-servers. Syst Biology 57 : 758 771.
80. Sullivan, M.B., Waterbury, J.B. Chisholm, S.W. (2003) Cyanophages infecting the oceanic cyanobacterium Prochlorococcus. Nature 424 : 1047 1051.
81. Sullivan, M.B., Coleman, M., Weigele, P., Rohwer, F. Chisholm, S.W. (2005) Three Prochlorococcus cyanophage genomes: signature features and ecological interpretations. PLoS Biol 3 : e144.
82. Sullivan, M.B., Lindell, D., Lee, J.A., Thompson, L.R., Bielawski, J.P. Chisholm, S.W. (2006) Prevalence and evolution of core photosystem II genes in marine cyanobacterial viruses and their hosts. PLoS Biol 4 : e234.
83. Suttle, C.A. Chan, A.M. (1994) Dynamics and distribution of cyanophages and their effects on marine Synechococcus spp. Appl Environ Microbiol 60 : 3167 3174.
84. Toleman, M.A., Bennett, P.M. Walsh, T.R. (2006) ISCR elements: novel gene-capturing systems of the 21st century? Microbiol Mol Biol Rev 70 : 296 316.
85. Tolonen, A.C., Aach, J., Lindell, D., Johnson, Z.I., Rector, T., Steen, R., et al. (2006) Global gene expression of Prochlorococcus ecotypes in response to changes in nitrogen availability. Mol Syst Biol 2 : 53.
86. Wagner, P.L. Waldor, M.K. (2002) Bacteriophage control of bacterial virulence. Infect Immun 70 : 3985 3993.
87. Waterbury, J.B. Valois, F.W. (1993) Resistance to co-occurring phages enables marine Synechococcus communities to coexist with cyanophage abundant in seawater. Appl Environ Microbiol 59 : 3393 3399.
88. Waterbury, J.B., Watson, S.W., Guillard, R.R.L. Brand, L.E. (1979) Widespread occurrence of a unicellular marine planktonic cyanobacterium. Nature 277 : 293 294.
89. Waterbury, J.B., Watson, S.W., Valois, F.W. Franks, D.G. (1986) Biological and ecological characterization of the marine unicellular cyanobacterium Synechococcus. Can Bull Fish Aquat Sci 214 : 71 120.
90. Weigele, P.R., Pope, W.H., Pedulla, M.L., Houtz, J.M., Smith, A.L., Conway, J.F., et al. (2007) Genomic and structural analysis of Syn9, a cyanophage infecting marine Prochlorococcus and Synechococcus. Environ Microbiol 9 : 1675 1695.
91. Whiteley, M., Bangera, M.G., Bumgarner, R.E., Parsek, M.R., Teitzel, G.M., Lory, S. Greenberg, E.P. (2001) Gene expression in Pseudomonas aeruginosa biofilms. Nature 413 : 860 864.
92. Williams, K.P. (2002) Integration sites for genetic elements in prokaryotic tRNA and tmRNA genes: sublocation preference of integrase subfamilies. Nucleic Acids Res 30 : 866 875.
93. Yoshida, T., Nagasaki, K., Takashima, Y., Shirai, Y., Tomaru, Y., Takao, Y., et al. (2008) Ma-LMM01 infecting toxic Microcystis aeruginosa illuminates diverse cyanophage genome strategies. J Bacteriol 190 : 1762 1772.
94. Zeidner, G., Bielawski, J.P., Shmoish, M., Scanlan, D.J., Sabehi, G. Beja, O. (2005) Potential photosynthesis gene recombination between Prochlorococcus and Synechococcus via viral intermediates. Environ Microbiol 7 : 1505 1513.