Biogeography of Viruses in the Sea

Annual Review of Virology

Volumn 2, Issue , 2015, Pages 41-66

  Chow, Cheryl Emiliane T ^a   Suttle, Curtis A ^a,b  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b CANADIAN INSTITUTE FOR ADVANCED RESEARCH   (Canada)

Author keywords

Biogeography; Community ecology; Marine; Metacommunity; Metagenomics; NCLDV; Phage; RNA virus

Indexed keywords

VIRUS DNA; VIRUS RNA; SEA WATER;

BIOGEOGRAPHY; COMMUNITY ECOLOGY; COMMUNITY STRUCTURE; CYANOPHAGE; HOST RANGE; MARINE VIRUS; METAGENOMICS; MICROBIAL COMMUNITY; MICROBIAL DIVERSITY; NONHUMAN; PRIORITY JOURNAL; PROCHLOROCOCCUS; REVIEW; RNA VIRUS; SEA; SINGLE-STRANDED DNA VIRUS; SYNECHOCOCCUS; VIRUS; VIRUS CELL INTERACTION; VIRUS GENOME; VIRUS PARTICLE; CLASSIFICATION; ECOLOGY; GENETICS; ISOLATION AND PURIFICATION; VIROLOGY;

ECOLOGY; SEAWATER; VIRUSES;

EID: 84969131071     PISSN: 2327056X     EISSN: 23270578     Source Type: Journal    
DOI: 10.1146/annurev-virology-031413-085540     Document Type: Review

References (154)

1. Winter C, Matthews B, Suttle CA. 2013. Effects of environmental variation and spatial distance on Bacteria, Archaea and viruses in sub-polar and arctic waters. ISME J. 7:1507-18
2. Brum JR, Sullivan MB. 2015. Rising to the challenge: Accelerated pace of discovery transforms marine virology. Nat. Rev. Microbiol. 13:147-59
3. Short SM, Suttle CA. 2002. Sequence analysis ofmarine virus communities reveals that groups of related algal viruses are widely distributed in nature. Appl. Environ. Microbiol. 68:1290-96
4. Breitbart M. 2012. Marine viruses: truth or dare. Annu. Rev. Mar. Sci. 4:425-48
5. Thurber RV. 2009. Current insights into phage biodiversity and biogeography. Curr. Opin. Microbiol. 12:582-87
6. Clokie MRJ, Millard AD, Letarov AV, Heaphy S. 2011. Phages in nature. Bacteriophage 1:31-45
7. Suttle CA. 2007. Marine viruses-major players in the global ecosystem. Nat. Rev. Microbiol. 5:801-12
8. Weitz JS, Wilhelm SW. 2012. Ocean viruses and their effects on microbial communities and biogeochemical cycles. F1000 Biol. Rep. 4:17
9. Mojica KDA, Brussaard CPD. 2014. Factors affecting virus dynamics and microbial host-virus interactions in marine environments. FEMS Microbiol. Ecol. 89:495-515
10. Angly FE, Felts B, Breitbart M, Salamon P, Edwards RA, et al. 2006. Themarine viromes of four oceanic regions. PLOS Biol. 4:2121-31
11. BreitbartM, Salamon P, Andresen B, Mahaffy JM, Segall AM, et al. 2002. Genomic analysis of uncultured marine viral communities. PNAS 99:14250-55
12. Hoffmann KH, Rodriguez-Brito B, Breitbart M, Bangor D, Angly FE, et al. 2007. Power law rankabundance models for marine phage communities. FEMS Microbiol. Lett. 273:224-28
13. Vage S, Storesund JE, Thingstad TF. 2013. Adding a cost of resistance description extends the ability of virus-host model to explain observed patterns in structure and function of pelagic microbial communities. Environ. Microbiol. 15:1842-52
14. Nemergut DR, Schmidt SK, Fukami T, O'Neill SP, Bilinski TM, et al. 2013. Patterns and processes of microbial community assembly. Microbiol. Mol. Biol. Rev. 77:342-56
15. Hanson CA, Fuhrman JA, Horner-Devine MC, Martiny JBH. 2012. Beyond biogeographic patterns: processes shaping the microbial landscape. Nat. Rev. Microbiol. 10:497-506
16. Leibold MA, Holyoak M, Mouquet N, Amarasekare P, Chase JM, et al. 2004. The metacommunity concept: A framework for multi-scale community ecology. Ecol. Lett. 7:601-13
17. Winegardner AK, Jones BK,NgISY, SiqueiraT,CottenieK. 2012. The terminology of metacommunity ecology. Trends Ecol. Evol. 27:253-54
18. Chow C-ET, Fuhrman JA. 2012. Seasonality and monthly dynamics of marine myovirus communities. Environ. Microbiol. 14:2171-83
19. Gustavsen JA, Winget DM,Tian X, SuttleCA. 2014. High temporal and spatial diversity in marine RNA viruses implies that they have an important role in mortality and structuring plankton communities. Front. Microbiol. 5:703
20. Amend AS,Oliver TA, Amaral-Zettler LA, Boetius A, Fuhrman JA, et al. 2013. Macroecological patterns of marine bacteria on a global scale. J. Biogeogr. 40:800-11
21. Brown MV, Lauro FM, DeMaere MZ, Muir L, Wilkins D, et al. 2012. Global biogeography of SAR11 marine bacteria. Mol. Syst. Biol. 8:595
22. Alonso C, Warnecke F, Amann R, Pernthaler J. 2007. High local and global diversity of Flavobacteria in marine plankton. Environ. Microbiol. 9:1253-66
23. Hellweger FL, van Sebille E, Fredrick ND. 2014. Biogeographic patterns in ocean microbes emerge in a neutral agent-based model. Science 345:1346-49
24. Pommier T, Canbäck B, Riemann L, Boström KH, Simu K, et al. 2007. Global patterns of diversity and community structure in marine bacterioplankton. Mol. Ecol. 16:867-80
25. Fuhrman JA, Steele JA, Hewson I, Schwalbach MS, Brown MV, et al. 2008. A latitudinal diversity gradient in planktonic marine bacteria. PNAS 105:7774-78
26. Martiny JBH, Bohannan BJM, Brown JH,Colwell RK, Fuhrman JA, et al. 2006. Microbial biogeography: putting microorganisms on the map. Nat. Rev. Microbiol. 4:102-12
27. De Wit R, Bouvier T. 2006. "Everything is everywhere, but, the environment selects"; what did Baas Becking and Beijerinck really say? Environ. Microbiol. 8:755-58
28. Logue JB, Mouquet N, Peter H, Hillebrand H, Metacommunity Working Group. 2011. Empirical approaches to metacommunities: A review and comparison with theory. Trends Ecol. Evol. 26:482-91
29. Bie T, Meester L, Brendonck L, Martens K, Goddeeris B, et al. 2012. Body size and dispersal mode as key traits determining metacommunity structure of aquatic organisms. Ecol. Lett. 15:740-47
30. Moritz C, Meynard CN, Devictor V, Guizien K, Labrune C, et al. 2013. Disentangling the role of connectivity, environmental filtering, and spatial structure onmetacommunity dynamics. Oikos 122:1401-10
31. Barbeŕan A, Casamayor EO, Fierer N. 2014. The microbial contribution to macroecology. Front. Microbiol. 5:203
32. LeiboldMA, Norberg J. 2004. Biodiversity in metacommunities: plankton as complex adaptive systems? Limnol. Oceanogr. 49:1278-89
33. Barbeŕan A, Casamayor EO. 2010. Global phylogenetic community structure and β-diversity patterns in surface bacterioplankton metacommunities. Aquat. Microb. Ecol. 59:1-10
34. Davies KF, HolyoakM, Preston KA, Offeman VA, Lum Q. 2009. Factors controlling community structure in heterogeneous metacommunities. J. Anim. Ecology 78:937-44
35. Langenheder S, Székely AJ. 2011. Species sorting and neutral processes are both important during the initial assembly of bacterial communities. ISME J. 5:1086-94
36. Sul WJ, Oliver TA, Ducklow HW, Amaral-Zettler LA, Sogin ML. 2013. Marine bacteria exhibit a bipolar distribution. PNAS 110:2342-47
37. Kellogg CA, Griffin DW. 2006. Aerobiology and the global transport of desert dust. Trends Ecol. Evol. 21:638-44
38. Aller JY, Kuznetsova MR, Jahns CJ, Kemp PF. 2005. The sea surface microlayer as a source of viral and bacterial enrichment in marine aerosols. J. Aerosol Sci. 36:801-12
39. Grossart H-P,Dziallas C, Leunert F,TangKW. 2010. Bacteria dispersal by hitchhiking on zooplankton. PNAS 107:11959-64
40. Lawrence JE, Suttle CA. 2004. Effect of viral infection on sinking rates of Heterosigma akashiwo and its implications for bloom termination. Aquat. Microb. Ecol. 37:1-7
41. Turner JT. 2002. Zooplankton fecal pellets, marine snow and sinking phytoplankton blooms. Aquat. Microb. Ecol. 27:57-102
42. Frada MJ, Schatz D, Farstey V, Ossolinski JE, Sabanay H, et al. 2014. Zooplankton may serve as transmission vectors for viruses infecting algal blooms in the ocean. Curr. Biol. 24:2592-97
43. WilkinsD, van Sebille E, Rintoul SR, Lauro FM,Cavicchioli R. 2013. Advection shapes Southern Ocean microbial assemblages independent of distance and environment effects. Nat. Commun. 4:2457
44. Suttle CA, Chan AM. 1994. Dynamics and distribution of cyanophages and their effect on marine Synechococcus spp. Appl. Environ. Microbiol. 60:3167-74
45. Wilhelm SW, JeffreyWH, Dean AL,Meador J, Pakulski JD, Mitchell DL. 2003. UV radiation induced DNA damage in marine viruses along a latitudinal gradient in the southeastern Pacific Ocean. Aquat. Microb. Ecol. 31:1-8
46. Weinbauer MG, Wilhelm SW, Suttle CA, Garza DR. 1997. Photoreactivation compensates for UV damage and restores infectivity to natural marine virus communities. Appl. Environ.Microbiol. 63:2200-5
47. Jacquet S, Bratbak G. 2003. Effects of ultraviolet radiation on marine virus-phytoplankton interactions. FEMS Microbiol. Ecol. 44:279-89
48. GarzaDR, SuttleCA. 1998. The effect of cyanophages on themortality of Synechococcus spp. and selection for UV resistant viral communities. Microb. Ecol. 36:281-92
49. WeinbauerMG, Brettar I, HöfleMG. 2003. Lysogeny and virus-induced mortality of bacterioplankton in surface, deep, and anoxic marine waters. Limnol. Oceanogr. 48:1457-65
50. Evans C, Brussaard CPD. 2012. Regional variation in lytic and lysogenic viral infection in the Southern Ocean and its contribution to biogeochemical cycling. Appl. Environ. Microbiol. 78:6741-48
51. Payet JP, Suttle CA. 2013. To kill or not to kill: The balance between lytic and lysogenic viral infection is driven by trophic status. Limnol. Oceanogr. 58:465-74
52. Wommack KE, Colwell RR. 2000. Virioplankton: viruses in aquatic ecosystems. Microbiol. Mol. Biol. Rev. 64:69-114
53. Motegi C, Kaiser K, Benner R, Weinbauer MG. 2015. Effect of P-limitation on prokaryotic and viral production in surface waters of the Northwestern Mediterranean Sea. J. Plankton Res. 37:16-20
54. Parada V, Herndl GJ, Weinbauer MG. 2006. Viral burst size of heterotrophic prokaryotes in aquatic systems. J. Mar. Biol. Assoc. 86:613-21
55. Kang I, Oh HM, Kang D, Cho JC. 2013. Genome of a SAR116 bacteriophage shows the prevalence of this phage type in the oceans. PNAS 110:12343-48
56. Zhao Y, Temperton B, Thrash JC, Schwalbach MS, Vergin KL, et al. 2013. Abundant SAR11 viruses in the ocean. Nature 494:357-60
57. 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. 32:506-16
58. Traving SJ, Clokie MRJ, Middelboe M. 2014. Increased acidification has a profound effect on the interactions between the cyanobacterium Synechococcus sp. WH7803 and its viruses. FEMS Microbiol. Ecol. 87:133-41
59. Short SM. 2012. The ecology of viruses that infect eukaryotic algae. Environ. Microbiol. 14:2253-71
60. Lindell D, Jaffe JD, Johnson ZI, Church GM, Chisholm SW. 2005. Photosynthesis genes in marine viruses yield proteins during host infection. Nature 438:86-89
61. Ignacio-Espinoza JC, Sullivan MB. 2012. Phylogenomics of T4 cyanophages: lateral gene transfer in the "core" and origins of host genes. Environ. Microbiol. 14:2113-26
62. Labrie SJ, Frois-Moniz K, Osburne MS, Kelly L, Roggensack SE, et al. 2013. Genomes of marine cyanopodoviruses reveal multiple origins of diversity. Environ. Microbiol. 15:1356-76
63. Monier A, Welsh RM, Gentemann C, Weinstock G, Sodergren E, et al. 2012. Phosphate transporters in marine phytoplankton and their viruses: cross-domain commonalities in viral-host gene exchanges. Environ. Microbiol. 14:162-76
64. Fischer MG, Allen MJ, Wilson WH, Suttle CA. 2010. Giant virus with a remarkable complement of genes infects marine zooplankton. PNAS 107:19508-13
65. Weynberg KD, Allen MJ, Gilg IC, Scanlan DJ, Wilson WH. 2011. Genome sequence of Ostreococcus tauri virus OtV-2 throws light on the role of picoeukaryote niche separation in the ocean. J. Virol. 85:4520-29
66. Hellweger FL. 2009. Carrying photosynthesis genes increases ecological fitness of cyanophage in silico. Environ. Microbiol. 11:1386-94
67. Waterbury JB, Valois FW. 1993. Resistance to co-occurring phages enables marine Synechococcus communities to coexist with cyanophages abundant in seawater. Appl. Environ. Microbiol. 59:3393-99
68. Sullivan MB, Waterbury JB, Chisholm SW. 2003. Cyanophages infecting the oceanic cyanobacterium Prochlorococcus. Nature 424:1047-51
69. 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
70. MarstonMF, Taylor S, SmeN, Parsons RJ,Noyes TJE, Martiny JBH. 2013. Marine cyanophages exhibit local and regional biogeography. FEMS Microbiol. Rev. 15:1452-63
71. CottrellMT, Suttle CA. 1991. Wide-spread occurrence and clonal variation in viruses which cause lysis of a cosmopolitan, eukaryotic marine phytoplankter, Micromonas pusilla. Mar. Ecol. Prog. Ser. 78:1-9
72. Tai V, Lawrence JE, Lang AS, Chan AM, Culley AI, Suttle CA. 2003. Characterization of HaRNAV, a single-stranded RNA virus causing lysis of Heterosigma akashiwo (Raphidophyceae). J. Phycol. 39:343-52
73. Tomaru Y, Katanozaka N, Nishida K, Shirai Y, Tarutani K, et al. 2004. Isolation and characterization of two distinct types of HcRNAV, a single-stranded RNA virus infecting the bivalve-killing microalga Heterocapsa circularisquama. Aquat. Microb. Ecol. 34:207-18
74. Clerissi C, Desdevises Y, Grimsley N. 2012. Prasinoviruses of the marine green alga Ostreococcus tauri are mainly species specific. J. Virol. 86:4611-19
75. Derelle E, Monier A, Cooke R, Worden AZ, Grimsley NH, Moreau H. 2015. Diversity of viruses infecting the green micro-alga Ostreococcus lucimarinus. J. Virol. 89:5812-21
76. Holmfeldt K,Middelboe M, Nybroe O, Riemann L. 2007. Large variabilities in host strain susceptibility and phage host range govern interactions between lytic marine phages and their Flavobacterium hosts. Appl. Environ. Microbiol. 73:6730-39
77. Nemergut DR, Costello EK, Hamady M, Lozupone C, Jiang L, et al. 2011. Global patterns in the biogeography of bacterial taxa. Environ. Microbiol. 13:135-44
78. Bergh Ø, Børsheim KY, Bratbak G, Heldal M. 1989. High abundance of viruses found in aquatic environments. Nature 340:467-68
79. Proctor LM, Fuhrman JA. 1990. Viral mortality ofmarine bacteria and cyanobacteria. Nature 343:60-62
80. Parsons RJ, Breitbart M, Lomas MW, Carlson CA. 2012. Ocean time-series reveals recurring seasonal patterns of virioplankton dynamics in the northwestern Sargasso Sea. ISME J. 6:273-84
81. Johannessen TV, Bratbak G, Larsen A, Ogata H, Egge ES, et al. 2015. Characterisation of three novel giant viruses reveals huge diversity among viruses infectingPrymnesiales (Haptophyta). Virology 476:180-88
82. Huang S,WangK, Jiao N, Chen F. 2012. Genome sequences of siphoviruses infectingmarine Synechococcus unveil a diverse cyanophage group and extensive phage-host genetic exchanges. Environ. Microbiol. 14:540-58
83. Holmfeldt K, Solonenko N, Shah M, Corrier K, Riemann L, et al. 2013. Twelve previously unknown phage genera are ubiquitous in global oceans. PNAS 110:12798-803
84. Mizuno CM, Rodriguez-Valera F, Kimes NE, Ghai R. 2013. Expanding the marine virosphere using metagenomics. PLOS Genet. 9:e1003987
85. Labonté JM, Suttle CA. 2013. Metagenomic and whole-genome analysis reveals new lineages of gokushoviruses and biogeographic separation in the sea. Front. Microbiol. 4:404
86. Adriaenssens EM, Cowan DA. 2014. Using signature genes as tools to assess environmental viral ecology and diversity. Appl. Environ. Microbiol. 80:4470-80
87. Sullivan MB, Coleman ML, Quinlivan V, Rosenkrantz JE, DeFrancesco AS, et al. 2008. Portal protein diversity and phage ecology. Environ. Microbiol. 10:2810-23
88. Bellec L, Grimsley N, Moreau H, Desdevises Y. 2009. Phylogenetic analysis of new Prasinoviruses (Phycodnaviridae) that infect the green unicellular algae Ostreococcus, Bathycoccus and Micromonas. Environ. Microbiol. Rep. 1:114-23
89. Culley AI, Steward GF. 2007. New genera of RNA viruses in subtropical seawater, inferred from polymerase gene sequences. Appl. Environ. Microbiol. 73:5937-44
90. Sakowski EG, Munsell EV, Hyatt M, Kress W, Williamson SJ, et al. 2014. Ribonucleotide reductases reveal novel viral diversity and predict biological and ecological features of unknown marine viruses. PNAS 111:15786-91
91. Schmidt HF, Sakowski EG,Williamson SJ, Polson SW,Wommack KE. 2014. Shotgun metagenomics indicates novel family A DNA polymerases predominate within marine virioplankton. ISME J. 8:103-14
92. Hurwitz BL,Brum JR, Sullivan MB. 2015. Depth-stratified functional and taxonomic niche specialization in the 'core' and 'flexible' Pacific Ocean Virome. ISME J. 9:472-84
93. Solonenko SA, Ignacio-Espinoza JC, Alberti A, Cruaud C, Hallam SJ, et al. 2013. Sequencing platform and library preparation choices impact viral metagenomes. BMC Genomics 14:320
94. Brum JR, Ignacio-Espinoza JC, Roux S, Doulcier G, Acinas SG, et al. 2015. Patterns and ecological drivers of ocean viral communities. Science 348:1261498
95. Hurwitz BL, Westveld AH, Brum JR, Sullivan MB. 2014. Modeling ecological drivers in marine viral communities using comparative metagenomics and network analyses. PNAS 111:10714-19
96. Hurwitz BL, Sullivan MB. 2013. The Pacific Ocean Virome (POV): A marine viral metagenomic dataset and associated protein clusters for quantitative viral ecology. PLOS ONE 8:e57355
97. Needham DM, Chow C-ET, Cram JA, Sachdeva R, Parada A, Fuhrman JA. 2013. Short-term observations ofmarine bacterial and viral communities: patterns, connections and resilience. ISME J. 7:1274-85
98. Chow C-ET, Kim DY, Sachdeva R, Caron DA, Fuhrman JA. 2014. Top-down controls on bacterial community structure: microbial network analysis of bacteria, T4-like viruses and protists. ISME J. 8:816-29
99. Weitz JS, Poisot T, Meyer JR, Flores CO, Valverde S, et al. 2013. Phage-bacteria infection networks. Trends Microbiol. 21:82-91
100. Martinez JM, Schroeder DC, Larsen A, Bratbak G, Wilson WH. 2007. Molecular dynamics of Emiliania huxleyi and cooccurring viruses during two separate mesocosm studies. Appl. Environ. Microbiol. 73:554-62
101. Tomaru Y, Tarutani K, Yamaguchi M, Nagasaki K. 2004. Quantitative and qualitative impacts of viral infection on a Heterosigma akashiwo (Raphidophyceae) bloom in Hiroshima Bay, Japan. Aquat. Microb. Ecol. 34:227-38
102. Short SM, Suttle CA. 2003. Temporal dynamics of natural communities of marine algal viruses and eukaryotes. Aquat. Microb. Ecol. 32:107-19
103. Holmfeldt K, Howard-Varona C, Solonenko N, Sullivan MB. 2014. Contrasting genomic patterns and infection strategies of two co-existing Bacteroidetes podovirus genera. Environ. Microbiol. 16:2501-13
104. Deng L, Ignacio-Espinoza JC, Gregory AC, Poulos BT, Weitz JS, et al. 2014. Viral tagging reveals discrete populations in Synechococcus viral genome sequence space. Nature 513:242-45
105. Chow C-ET,Winget DM, White RA III, Hallam SJ, Suttle CA. 2015. Combining genomic sequencing methods to explore viral diversity and reveal potential virus-host interactions. Front. Microbiol. 6:265
106. Martinez JM, Swan BK, Wilson WH. 2014. Marine viruses, a genetic reservoir revealed by targeted viromics. ISME J. 8:1079-88
107. Roux S, Hawley AK, Torres Beltran M, Scofield M, Schwientek P, et al. 2014. Ecology and evolution of viruses infecting uncultivated SUP05 bacteria as revealed by single-cell-and meta-genomics. eLife 3:e03125
108. Labonté JM, Swan BK, Poulos B, Luo H, Koren S, et al. 2015. Single-cell genomics-based analysis of virus-host interactions in marine surface bacterioplankton. ISME J. doi: 10.1038/ismej.2015.48
109. Breitbart M, Miyake JH, Rohwer F. 2004. Global distribution of nearly identical phage-encoded DNA sequences. FEMS Microbiol. Lett. 236:249-56
110. Clasen JL, Hanson CA, Ibrahim Y, Weihe C. 2013. Diversity and temporal dynamics of Southern California coastal marine cyanophage isolates. Aquat. Microb. Ecol. 69:17-31
111. Kang I, Cho J-C. 2014. Depth-specific distribution of the SAR116 phages revealed by virome binning. J. Microbiol. Biotechnol. 24:592-96
112. Lindell D, Jaffe JD, Coleman ML, Futschik ME, Axmann IM, et al. 2007. Genome-wide expression dynamics of a marine virus and host reveal features of co-evolution. Nature 449:83-86
113. Thompson LR, Zeng Q, Kelly L, Huang KH, Singer AU, et al. 2011. Phage auxiliary metabolic genes and the redirection of cyanobacterial host carbon metabolism. PNAS 108:E757-64
114. Zwirglmaier K, Jardillier L, Ostrowski M, Mazard S,Garczarek L, et al. 2008. Global phylogeography of marine Synechococcus and Prochlorococcus reveals a distinct partitioning of lineages among oceanic biomes. Environ. Microbiol. 10:147-61
115. Malmstrom RR, Coe A, Kettler GC, Martiny AC, Frias-Lopez J, et al. 2010. Temporal dynamics of Prochlorococcus ecotypes in the Atlantic and Pacific oceans. ISME J. 4:1252-64
116. Martiny AC, Tai APK, Veneziano D, Primeau F, Chisholm SW. 2009. Taxonomic resolution, ecotypes and the biogeography of Prochlorococcus. Environ. Microbiol. 11:823-32
117. JamesonE,MannNH, Joint I, Sambles C,MühlingM. 2011.The diversity of cyanomyovirus populations along a North-South Atlantic Ocean transect. ISME J. 5:1713-21
118. Wilson WH, Fuller NJ, Joint IR, Mann NH. 1999. Analysis of cyanophage diversity and population structure in a south-north transect of the Atlantic Ocean. Bull. Inst. Oceanogr. Monaco 19:209-16
119. Green JL, Bohannan BJM,Whitaker RJ. 2008. Microbial biogeography: from taxonomy to traits. Science 320:1039-43
120. Barton AD, Pershing AJ, Litchman E, Record NR, Edwards KF, et al. 2013. The biogeography of marine plankton traits. Ecol. Lett. 16:522-34
121. Sharon I, Battchikova N, Aro E-M, Giglione C, Meinnel T, et al. 2011. Comparative metagenomics of microbial traits within oceanic viral communities. ISME J. 5:1178-90
122. Sharon I, Tzahor S, Williamson SJ, Shmoish M, Man-Aharonovich D, et al. 2007. Viral photosynthetic reaction center genes and transcripts in the marine environment. ISME J. 1:492-501
123. Chenard C, Suttle CA. 2008. Phylogenetic diversity of sequences of cyanophage photosynthetic gene psbA in marine and freshwaters. Appl. Environ. Microbiol. 74:5317-24
124. Verreydt D, De Meester L, Decaestecker E, Villena M-J, Van Der Gucht K, et al. 2012. Dispersalmediated trophic interactions can generate apparent patterns of dispersal limitation in aquaticmetacommunities. Ecol. Lett. 15:218-26
125. Williamson SJ, Rusch DB, Yooseph S, Halpern AL, Heidelberg KB, et al. 2008. The Sorcerer II Global Ocean Sampling Expedition: metagenomic characterization of viruses within aquatic microbial samples. PLOS ONE 3:e1456
126. Huang S, Zhang S, Jiao N, Chen F. 2015. Marine cyanophages demonstrate biogeographic patterns throughout the global ocean. Appl. Environ. Microbiol. 81:441-52
127. Roux S, Tournayre J, Mahul A, Debroas D, Enault F. 2014. Metavir 2: new tools for viral metagenome comparison and assembled virome analysis. BMC Bioinform. 15:76
128. Dinsdale EA, Pantos O, Smriga S, Edwards RA, Angly FE, et al. 2008. Microbial ecology of four coral atolls in the Northern Line Islands. PLOS ONE 3:e1584
129. Williamson SJ, Allen LZ, Lorenzi HA, Fadrosh DW, Brami D, et al. 2012. Metagenomic exploration of viruses throughout the Indian Ocean. PLOS ONE 7:e42047
130. Cassman N, Prieto-Davó A, Walsh K, Silva GGZ, Angly FE, et al. 2012. Oxygen minimum zones harbour novel viral communities with low diversity. Environ. Microbiol. 14:3043-65
131. Sullivan MB, Coleman ML, Weigele P, Rohwer F, Chisholm SW. 2005. Three Prochlorococcus cyanophage genomes: signature features and ecological interpretations. PLOS Biol. 3:790-806
132. Follows MJ, Dutkiewicz S, Grant S, Chisholm SW. 2007. Emergent biogeography of microbial communities in a model ocean. Science 315:1843-46
133. Monier A, Comte J, Babin M, Forest A, Matsuoka A, Lovejoy C. 2015. Oceanographic structure drives the assembly processes of microbial eukaryotic communities. ISME J. 9:990-1002
134. Rodríguez-Ramos T, Mara nón E, Cermeno P. 2015. Marine nano-and microphytoplankton diversity: redrawing global patterns from sampling-standardized data. Glob. Ecol. Biogeogr. 24:527-38
135. Monier A, Claverie J-MM, Ogata H. 2008. Taxonomic distribution of large DNA viruses in the sea. Genome Biol. 9:R106
136. Bellec L, Clerissi C, Edern R, Foulon E, Simon N, et al. 2014. Cophylogenetic interactions between marine viruses and eukaryotic picophytoplankton. BMC Evol. Biol. 14:59
137. Derelle E, Ferraz C, Escande M-L, Eychenié S, Cooke R, et al. 2008. Life-cycle and genome of OtV5, a large DNA virus of the pelagic marine unicellular green alga Ostreococcus tauri. PLOS ONE 3:e2250
138. Waters RE, Chan AT. 1982. Micromonas pusilla virus: The virus growth cycle and associated physiological events within the host cells; host range mutation. J. Gen. Virol. 63:199-206
139. Clerissi C, Grimsley N, Ogata H, Hingamp P, Poulain J, Desdevises Y. 2014. Unveiling of the diversity of prasinoviruses (Phycodnaviridae) in marine samples by using high-throughput sequencing analyses of PCR-amplified DNA polymerase and major capsid protein genes. Appl. Environ. Microbiol. 80:3150-60
140. Clerissi C, Grimsley N, Subirana L, Maria E, Oriol L, et al. 2014. Prasinovirus distribution in the Northwest Mediterranean Sea is affected by the environment and particularly by phosphate availability. Virology 466-67:146-57
141. Steward GF, Culley AI, Mueller JA, Wood-Charlson EM, Belcaid M, Poisson G. 2013. Are we missing half of the viruses in the ocean? ISME J. 7:672-79
142. Lang AS, RiseML, Culley AI, Steward GF. 2009. RNA viruses in the sea. FEMS Microbiol. Rev. 33:295-323
143. Nagasaki K, Tomaru Y, Katanozaka N, Shirai Y, Nishida K, et al. 2004. Isolation and characterization of a novel single-stranded RNA virus infecting the bloom-forming diatom Rhizosolenia setigera. Appl. Environ. Microbiol. 70:704-11
144. Shirai Y, Tomaru Y, Takao Y, Suzuki H, Nagumo T, Nagasaki K. 2008. Isolation and characterization of a single-stranded RNA virus infecting the marine planktonic diatom Chaetoceros tenuissimus Meunier. Appl. Environ. Microbiol. 74:4022-27
145. Tomaru Y, Hata N, Masuda T, Tsuji M, Igata K, et al. 2007. Ecological dynamics of the bivalve-killing dinoflagellate Heterocapsa circularisquama and its infectious viruses in different locations of western Japan. Environ. Microbiol. 9:1376-83
146. Attoui H, Jaafar FM, Belhouchet M, de Micco P, de Lamballerie X, Brussaard CPD. 2006. Micromonas pusilla reovirus: A newmember of the family Reoviridae assigned to a novel proposed genus (Mimoreovirus). J. Gen. Virol. 87:1375-83
147. Culley AI, Lang AS, Suttle CA. 2006. Metagenomic analysis of coastal RNA virus communities. Science 312:1795-98
148. Rosario K, Duffy S, Breitbart M. 2009. Diverse circovirus-like genome architectures revealed by environmental metagenomics. J. Gen. Virol. 90:2418-24
149. Tucker KP, Parsons R, Symonds EM, Breitbart M. 2010. Diversity and distribution of single-stranded DNA phages in the North Atlantic Ocean. ISME J. 5:822-30
150. Roux S, Krupovic M, Poulet A, Debroas D, Enault F. 2012. Evolution and diversity of the Microviridae viral family through a collection of 81 new complete genomes assembled from virome reads. PLOS ONE 7:e40418
151. Labonté JM, Suttle CA. 2013. Previously unknown and highly divergent ssDNA viruses populate the oceans. ISME J. 7:2169-77
152. Labonté JM, Hallam SJ, SuttleCA. 2015. Previously unknown evolutionary groups dominate the ssDNA gokushoviruses in oxic and anoxic waters of a coastal marine environment. Front. Microbiol. 6:315
153. Krupovic M, Forterre P. 2015. Single-stranded DNA viruses employ a variety of mechanisms for integration into host genomes. Ann. N.Y. Acad. Sci. 1341:41-53
154. Thingstad TF, Vage S, Storesund JE, Sandaa R-A, Giske J. 2014. A theoretical analysis of how strainspecific viruses can control microbial species diversity. PNAS 111:7813-18