Prevalence and evolution of core photosystem II genes in marine cyanobacterial viruses and their hosts

PLoS Biology

Volumn 4, Issue 8, 2006, Pages 1344-1357

  Sullivan, Matthew B ^a   Lindell, Debbie ^a   Lee, Jessica A ^b   Thompson, Luke R ^b   Bielawski, Joseph P ^c   Chisholm, Sallie W ^a,b  

^a Massachusetts Institute of Technology Cambridge   (United States)

^b MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^c DALHOUSIE UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CORE PROTEIN; MOLECULAR MARKER; VIRUS DNA; PHOTOSYSTEM II, PSBA SUBUNIT;

ARTICLE; BACTERIAL GENE; BACTERIOPHAGE; BACTERIOPLANKTON; CONTROLLED STUDY; CYANOBACTERIUM; DNA SCREENING; GENE SEQUENCE; GENE TRANSFER; GENETIC RECOMBINATION; GENETIC VARIABILITY; HOST SELECTION; INFECTION RATE; MOLECULAR EVOLUTION; NONHUMAN; NUCLEOTIDE SEQUENCE; PHOTOSYSTEM II; PHYLOGENY; PREVALENCE; PROCHLOROCOCCUS; PSBA GENE; PSBD GENE; SYNECHOCOCCUS; VIRUS; CLASSIFICATION; DNA BASE COMPOSITION; EVOLUTION; GENETICS; HORIZONTAL GENE TRANSFER; MOLECULAR GENETICS; PATHOGENICITY; PHOTOSYNTHESIS; VIROLOGY; VIRUS GENOME;

CYANOBACTERIA; PROCHLOROCOCCUS; SYNECHOCOCCUS;

BASE COMPOSITION; CAUDOVIRALES; EVOLUTION; GENE TRANSFER, HORIZONTAL; GENOME, VIRAL; MOLECULAR SEQUENCE DATA; PHOTOSYNTHETIC REACTION CENTER COMPLEX PROTEINS; PHOTOSYSTEM II PROTEIN COMPLEX; PHYLOGENY; PROCHLOROCOCCUS; SYNECHOCOCCUS;

EID: 33747369803     PISSN: 15457885     EISSN: 15457885     Source Type: Journal    
DOI: 10.1371/journal.pbio.0040234     Document Type: Article

References (84)

1. Waterbury JB, Watson SW, Valois FW, Franks DG (1986) Biological and ecological characterization of the marine unicellular cyanobacterium Synechococcus. Can Bull Fish Aquat Sci 214: 71-120.
2. Partensky F,HessWR, VaulotD(1999) Prochlorococcus, a marine photosynthetic prokaryote of global significance. Microbiol Mol Biol Rev 63: 106-127.
3. Suttle CA, Chan AM (1994) Dynamics and distribution of cyanophages and their effects on marine Synechococcus spp. Appl Environ Microbiol 60: 3167-3174.
4. Waterbury JB, Valois FW (1993) Resistance to co-occurring phages enables marine Synechococcus communities to coexist with cyanophage abundant in seawater. Appl Environ Microbiol 59: 3393-3399.
5. Sullivan MB, Waterbury JB, Chisholm SW (2003) Cyanophages infecting the oceanic cyanobacterium Prochlorococcus. Nature 424: 1047-1051.
6. Lu J, Chen F, Hodson RE (2001) Distribution, isolation, host specificity, and diversity of cyanophages infecting marine Synechococcus spp. in river estuaries. Appl Environ Microbiol 67: 3285-3290.
7. Marston MF, Sallee JL (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.
8. Muhling M, Fuller NJ, Millard A, Somerfield PJ, Marie D, et al. (2005) Genetic diversity of marine Synechococcus and co-occurring cyanophage communities: Evidence for viral control of phytoplankton. Environ Microbiol 7: 499-508.
9. Wilson WH, Joint IR, Carr NG, Mann NH (1993) Isolation and molecular characterization of five marine cyanophages propogated on Synechococcus sp. strain WH 7803. Appl Environ Microbiol 59: 3736-3743.
10. Suttle CA, Chan AM (1993) Marine cyanophages infecting oceanic and coastal strains of Synechococcus: Abundance, morphology, cross-infectivity and growth characteristics. Mar Ecol Prog Ser 92: 99-109.
11. Brussow H, Canchaya C, Hardt WD (2004) Phages and the evolution of bacterial pathogens: From genomic rearrangements to lysogenic conversion. Microbiol Mol Biol Rev 68: 560-602.
12. Faruque SM, Mekalanos JJ (2003) Pathogenicity islands and phages in Vibrio cholerae evolution. Trends Microbiol 11: 505-510.
13. Lindell D, Sullivan MB, Johnson ZI, Tolonen AC, Rohwer F, et al. (2004) Transfer of photosynthesis genes to and from Prochlorococcus viruses. Proc Natl Acad Sci U S A 101: 11013-11018.
14. Canchaya C, Proux C, Fournous G, Bruttin A, Brussow H (2003) Prophage genomics. Microbiol Mol Biol Rev 67: 238-276.
15. Casjens S (2003) Prophages and bacterial genomics: What have we learned so far? Mol Microbiol 49: 277-300.
16. Forterre P (1999) Displacement of cellular proteins by functional analogues from plasmids or viruses could explain puzzling phylogenies of many DNA informational proteins. Mol Microbiol 33: 457-465.
17. Filee J, Forterre P, Laurent J (2003) The role played by viruses in the evolution of their hosts: A view based on informational protein phylogenies. Res Microbiol 154: 237-243.
18. Filee J, Forterre P, Sen-Lin T, Laurent J (2002) Evolution of DNA polymerase families: Evidences for multiple gene exchange between cellular and viral proteins. J Mol Evol 54: 763-773.
19. Hendrix RW (1999) Evolution: The long evolutionary reach of viruses. Curr Biol 9: R914-917.
20. Hendrix RW, Lawrence JG, Hatfull GF, Casjens S (2000) The origins and ongoing evolution of viruses. Trends Microbiol 8: 504-508.
21. Juhala RJ, Ford ME, Duda RL, Youlton A, Hatfull GF, et al. (2000) Genomic sequences of bacteriophages HK97 and HK022: Pervasive genetic mosaicism in the lambdoid bacteriophages. J Mol Biol 299: 27-51.
22. Mann NH, Cook A, Millard A, Bailey S, Clokie M (2003) Bacterial photosynthesis genes in a virus. Nature 424: 741.
23. Botstein D (1980) A theory of modular evolution for bacteriophages. Ann New York Acad Sci 354: 484-491.
24. Hendrix RW, Smith MC, Burns RN, Ford ME, Hatfull GF (1999) Evolutionary relationships among diverse bacteriophages and prophages: All the world's a phage. Proc Natl Acad Sci U S A 96: 2192-2197.
25. Silander OK, Weinreich DM, Wright KM, O'Keefe KJ, Rang CU, et al. (2005) Widespread genetic exchange among terrestrial bacteriophages. Proc Natl Acad Sci U S A 102: 19009-19014.
26. Filee J, Tetart F, Suttle CA, Krisch HM (2005) Marine T4-type bacteriophages, a ubiquitous component of the dark matter of the biosphere. Proc Natl Acad Sci U S A.
27. Breitbart M, Miyake JH, Rohwer F (2004) Global distribution of nearly identical phage-encoded DNA sequences. FEMS Microbiol Lett 236: 249-256.
28. Mann NH, Clokie MR, Millard A, Cook A, Wilson WH, et al. (2005) The genome of S-PM2, a "photosynthetic" T4-type bacteriophage that infects marine Synechococcus. J Bacteriol 187: 3188-3200.
29. Millard A, Clokie MR, Shub DA, Mann NH (2004) Genetic organization of the psbAD region in phages infecting marine Synechococcus strains. Proc Natl Acad Sci U S A 101: 11007-11012.
30. Sullivan MB, Coleman M, Weigele P, Rohwer F, Chisholm SW (2005) Three Prochlorococcus cyanophage genomes: Signature features and ecological interpretations. PLoS Biol 3: e144. DOI: 10.1371/journal.pbio.0030144
31. Lindell D, Jaffe JD, Johnson ZI, Church GM, Chisholm SW (2005) Photosynthesis genes in marine viruses yield proteins during host infection. Nature 438: 8689.
32. Clokie MRJ, Shan J, Bailey S, Jia Y, Krisch HM (2006) Transcription of a 'photosynthetic' T4-type phage during infection of a marine cyanobacterium. Environ Microbiol 8: 827-835.
33. Benson R, Martin E (1981) Effects of photosynthetic inhibitors and lightdark regimes on the replication of cyanophage SM-2. Arch Microbiol 129: 165-167.
34. Adir N, Zer H, Schochat S, Ohad I (2003) Photoinhibition - A historical perspective. Photosynth Res 76: 343-370.
35. Paul JH, Sullivan MB (2005) Marine phage genomics: What have we learned? Curr Opin Biotechnol 16: 299-307.
36. 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.
37. Zeidner G, Bielawski JP, Shmoish M, Scanlan DJ, Sabehi G, et al. (2005) Potential photosynthesis gene recombination between Prochlorococcus and Synechococcus via viral intermediates. Environ Microbiol 7: 1505-1513.
38. Sherman LA (1976) Infection of Synechococcus cedrorum by the cyanophage AS-1M. III. Cellular metabolism and phage development. Virology 71: 199-206.
39. Wilson WH, Carr NG, Mann NH (1996) The effect of phosphate status on the kinetics of cyanophage infection in the oceanic cyanobacterium Synechococcus sp. WH7803. J Phycol 32: 506-516.
40. Levin BR, Lenski RE (1983) Coevolution in bacteria and their viruses and plasmids. In: Futuyma DJ, Slatkin M, editors. Coevolution. Sunderland (Massachusetts): Sinauer. pp. 99-127.
41. Wang IN, Dykhuizen DE, Slobodkin LB (1996) The evolution of phage lysis timing. Evol Ecol 10: 545-558.
42. Abedon ST (1989) Selection for bacteriophage latent period length by bacterial density: A theoretical examination. Microb Ecol 18: 79-88.
43. Abedon ST, Herschler TD, Stopar D (2001) Bacteriophage latent-period evolution as a response to resource availability. Appl Environ Microbiol 67: 4233-4241.
44. Abedon ST, Hyman P, Thomas C (2003) Experimental examination of bacteriophage latent-period evolution as a response to bacterial availability. Appl Environ Microbiol 69: 7499-7506.
45. Moore LR, Rocap G, Chisholm SW (1998) Physiology and molecular phylogeny of coexisting Prochlorococcus ecotypes. Nature 393: 464-467.
46. Lindell D, Penno S, Al-Qutob M, David E, Rivlin T, et al. (2005) Expression of the nitrogen stress response gene ntcA reveals nitrogen-sufficient Synechococcus populations in the oligotrophic northern Red Sea. Limnol and Oceanogr 50: 1932-1944.
47. Palenik B (2001) Chromatic adaptation in marine Synechococcus strains. Appl Environ Microbiol 67: 991-994.
48. Rocap G, Distel D, Waterbury JB, Chisholm SW (2002) Resolution of Prochlorococcus and Synechococcus ecotypes by using 16S-23S ribosomal DNA internal transcribed spacer sequences.Appl Environ Microbiol 68: 1180-1191.
49. Fuller NJ, Marie D, Partensky F, Vaulot D, Post AF, et al. (2003) Clade-specific 16S ribosomal DNA oligonucleotides reveal the predominance of a single marine Synechococcus clade throughout a stratified water column in the Red Sea. Appl Environ Microbiol 69: 2430-2443.
50. Golden SS, Brusslan J, Haselkorn R (1986) Expression of a family of psbA genes encoding a photosystem II polypeptide in the cyanobacterium Anacystis nidulans R2. Embo J 5: 2789-2798.
51. Sicora CI, Appleton SE, Brown CM, Chung J, Chandler J, et al. (2006) Cyanobacterial psbA families in Anabaena and Synechocystis encode trace, constitutive and UVB-induced D1 isoforms. Biochim Biophys Acta 1757: 47-56.
52. Clarke AK, Soitamo A, Gustafsson P, Oquist G (1993) Rapid interchange between two distinct forms of cyanobacterial photosystem II reaction-center protein D1 in response to photoinhibition. Proc Natl Acad Sci U S A 90: 9973-9977.
53. Hess WR, Weihe A, Loiseaux-de Goer S, Partensky F, Vaulot D (1995) Characterization of the single psbA gene of Prochlorococcus marinus CCMP1375 (Prochlorophyta). Plant Mol Biol 27: 1189-1196.
54. Calendar R (1988) The bacteriophages. New York: Plenum.
55. Ackermann HW, DuBow MS (1987) Viruses of prokaryotes, Volume 1. General properties of bacteriophages. Boca Raton (Florida): CRC Press.
56. Karl DM (1999) A sea of change: Biogeochemical variability in the North Pacific Subtropical Gyre. Ecosystems 2: 181-214.
57. Zinser ER, Coe A, Johnson ZI, Martiny AC, Fuller NJ, et al. (2006) Prochlorococcus ecotype abundances in the North Atlantic Ocean as revealed by an improved quantitative PCR method. Appl Environ Microbiol 72: 723-732.
58. Dufresne A, Salanoubat M, Partensky F, Artiguenave F, Axmann IM, et al. (2003) Genome sequence of the cyanobacterium Prochlorococcus marinus SS120, a nearly minimal oxyphototrophic genome. Proc Natl Acad Sci U S A 100: 10020-10025.
59. Palenik B, Brahamsha B, McCarren J, Waterbury J, Allen E, et al. (2003) The genome of a motile marine Synechococcus. Nature 424: 1037-1041.
60. Rocap G, Larimer FW, Lamerdin J, Malfatti S, Chain P, et al. (2003) Genome divergence in two Prochlorococcus ecotypes reflects oceanic niche differentiation. Nature 424: 1042-1047.
61. Zeidner G, Preston CM, Delong EF, Massana R, Post AF, et al. (2003) Molecular diversity among marine picophytoplankton as revealed by psbA analyses. Environ Microbiol 5: 212-216.
62. Thompson JR, Marcelino LA, Polz MF (2002) Heteroduplexes in mixed-template amplifications: Formation, consequence and elimination by 'reconditioning PCR.' Nucleic Acids Res 30: 2083-2088.
63. Coleman ML, Sullivan MB, Martiny AC, Steglich C, Barry K, et al. (2006) Genomic islands and the ecology and evolution of Prochlorococcus. Science 311: 1768-1770.
64. Hess WR, Rocap G, Ting CS, Larimer FW, Stilwagen S, et al. (2001) The photosynthetic apparatus of Prochlorococcus: Insights through comparative genomics. Photosynth Res 70: 53-71.
65. Acinas SG, Sarma-Rupavtarm R, Klepac-Ceraj V, Polz MF (2005) PCR-induced sequence artifacts and bias: Insights from comparison of two 16S rRNA clone libraries constructed from the same sample. Appl Environ Microbiol 71: 8966-8969.
66. Saitou N, Nei M (1987) The neighbor-joining method: A new method for reconstructing phylogenetic trees. Mol Biol Evol 4: 406-425.
67. Hasegawa M, Kishino H, Yano T (1985) Dating of the human-ape splitting by a molecular clock of mitochondrial DNA. J Mol Evol 22: 160-174.
68. Yang Z (1994) Maximum likelihood phylogenetic estimation from DNA sequences with variable rates over sites: Approximate methods. J Mol Evol 39: 306-314.
69. Schmidt HA, Strimmer K, Vingron M, von Haeseler A (2002) TREE-PUZZLE: Maximum likelihood phylogenetic analysis using quartets and parallel computing. Bioinformatics 18: 502-504.
70. Phillips MJ, Delsuc F, Penny D (2004) Genome-scale phylogeny and the detection of systematic biases. Mol Biol Evol 21: 1455-1458.
71. Kennedy M, Holland BR, Gray RD, Spencer HG (2005) Untangling long branches: Identifying conflicting phylogenetic signals using spectral analysis, neighbor-net, and consensus networks. Syst Biol 54: 620-633.
72. Bryant D, Moulton V (2004) Neighbor-net: An agglomerative method for the construction of phylogenetic networks. Mol Biol Evol 21: 255-265.
73. Huson DH, Bryant D (2006) Application of phylogenetic networks in evolutionary studies. Mol Biol Evol 23: 254-267.
74. Felsenstein J (1978) Cases in which parsimony or compatibility methods will be positively misleading. Syst Zool 27: 401-410.
75. Lockhart PJ, Steel M, Hendy MD, Penny D (1994) Recovering evolutionary trees under a more realistic model of sequence evolution. Mol Biol Evol 11: 605-612.
76. Schierup MH, Hein J (2000) Consequences of recombination on traditional phylogenetic analysis. Genetics 156: 879-891.
77. Yang Z, Roberts D (1995) On the use of nucleic acid sequences to infer early branchings in the tree of life. Mol Biol Evol 12: 451-458.
78. Padidam M, Sawyer S, Fauquet CM (1999) Possible emergence of new geminiviruses by frequent recombination. Virology 265: 218-225.
79. Maynard Smith J (1992) Analyzing the mosaic structure of genes. J Mol Evol 34: 126-129.
80. Posada D, Crandall KA (2001) Evaluation of methods for detecting recombination from DNA sequences: Computer simulations. Proc Natl Acad Sci U S A 98: 13757-13762.
81. Martin D, Rybicki E (2000) RDP: Detection of recombination amongst aligned sequences. Bioinformatics 16: 562-563.
82. Yang Z (1997) PAML: A program package for phylogenetic analysis by maximum likelihood. Comput Appl Biosci 13: 555-556.
83. Kishino H, Hasegawa M (1989) Evaluation of the maximum likelihood estimate of the evolutionary tree topologies from DNA sequence data, and the branching order in hominoidea. J Mol Evol 29: 170-179.
84. Shimodaira H, Hasegawa M (1999) Multiple comparisons of log-likelihoods and combining nonnested models with applications to phylogenetic inference. Mol Biol Evol 16: 1114-1116.