Viral ecology is a rapidly progressing area of research, as molecular methods have improved significantly for targeted research on specific populations and whole communities. To interpret and synthesize global viral diversity and distribution, it is feasible to assess whether macroecology concepts can apply to marine viruses. We review how viral and host life history and physical properties can influence viral distribution in light of biogeography and metacommunity ecology paradigms. We highlight analytical approaches that can be applied to emerging global data sets and meta-analyses to identify individual taxa with global influence and drivers of emergent properties that influence microbial community structure by drawing on examples across the spectrum of viral taxa, from RNA to ssDNA and dsDNA viruses.


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Literature Cited

  1. Winter C, Matthews B, Suttle CA. 1.  2013. Effects of environmental variation and spatial distance on Bacteria, Archaea and viruses in sub-polar and arctic waters. ISME J 7:1507–18 [Google Scholar]
  2. Brum JR, Sullivan MB. 2.  2015. Rising to the challenge: Accelerated pace of discovery transforms marine virology. Nat. Rev. Microbiol. 13:147–59 [Google Scholar]
  3. Short SM, Suttle CA. 3.  2002. Sequence analysis of marine virus communities reveals that groups of related algal viruses are widely distributed in nature. Appl. Environ. Microbiol. 68:1290–96 [Google Scholar]
  4. Breitbart M. 4.  2012. Marine viruses: truth or dare. Annu. Rev. Mar. Sci. 4:425–48 [Google Scholar]
  5. Thurber RV. 5.  2009. Current insights into phage biodiversity and biogeography. Curr. Opin. Microbiol. 12:582–87 [Google Scholar]
  6. Clokie MRJ, Millard AD, Letarov AV, Heaphy S. 6.  2011. Phages in nature. Bacteriophage 1:31–45 [Google Scholar]
  7. Suttle CA. 7.  2007. Marine viruses—major players in the global ecosystem. Nat. Rev. Microbiol. 5:801–12 [Google Scholar]
  8. Weitz JS, Wilhelm SW. 8.  2012. Ocean viruses and their effects on microbial communities and biogeochemical cycles. F1000 Biol. Rep. 4:17 [Google Scholar]
  9. Mojica KDA, Brussaard CPD. 9.  2014. Factors affecting virus dynamics and microbial host-virus interactions in marine environments. FEMS Microbiol. Ecol. 89:495–515 [Google Scholar]
  10. Angly FE, Felts B, Breitbart M, Salamon P, Edwards RA. 10.  et al. 2006. The marine viromes of four oceanic regions. PLOS Biol 4:2121–31 [Google Scholar]
  11. Breitbart M, Salamon P, Andresen B, Mahaffy JM, Segall AM. 11.  et al. 2002. Genomic analysis of uncultured marine viral communities. PNAS 99:14250–55 [Google Scholar]
  12. Hoffmann KH, Rodriguez-Brito B, Breitbart M, Bangor D, Angly FE. 12.  et al. 2007. Power law rank-abundance models for marine phage communities. FEMS Microbiol. Lett. 273:224–28 [Google Scholar]
  13. Vage S, Storesund JE, Thingstad TF. 13.  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 [Google Scholar]
  14. Nemergut DR, Schmidt SK, Fukami T, O'Neill SP, Bilinski TM. 14.  et al. 2013. Patterns and processes of microbial community assembly. Microbiol. Mol. Biol. Rev. 77:342–56 [Google Scholar]
  15. Hanson CA, Fuhrman JA, Horner-Devine MC, Martiny JBH. 15.  2012. Beyond biogeographic patterns: processes shaping the microbial landscape. Nat. Rev. Microbiol. 10:497–506 [Google Scholar]
  16. Leibold MA, Holyoak M, Mouquet N, Amarasekare P, Chase JM. 16.  et al. 2004. The metacommunity concept: a framework for multi-scale community ecology. Ecol. Lett. 7:601–13 [Google Scholar]
  17. Winegardner AK, Jones BK, Ng ISY, Siqueira T, Cottenie K. 17.  2012. The terminology of metacommunity ecology. Trends Ecol. Evol. 27:253–54 [Google Scholar]
  18. Chow C-ET, Fuhrman JA. 18.  2012. Seasonality and monthly dynamics of marine myovirus communities. Environ. Microbiol. 14:2171–83 [Google Scholar]
  19. Gustavsen JA, Winget DM, Tian X, Suttle CA. 19.  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 [Google Scholar]
  20. Amend AS, Oliver TA, Amaral-Zettler LA, Boetius A, Fuhrman JA. 20.  et al. 2013. Macroecological patterns of marine bacteria on a global scale. J. Biogeogr. 40:800–11 [Google Scholar]
  21. Brown MV, Lauro FM, DeMaere MZ, Muir L, Wilkins D. 21.  et al. 2012. Global biogeography of SAR11 marine bacteria. Mol. Syst. Biol. 8:595 [Google Scholar]
  22. Alonso C, Warnecke F, Amann R, Pernthaler J. 22.  2007. High local and global diversity of Flavobacteria in marine plankton. Environ. Microbiol. 9:1253–66 [Google Scholar]
  23. Hellweger FL, van Sebille E, Fredrick ND. 23.  2014. Biogeographic patterns in ocean microbes emerge in a neutral agent-based model. Science 345:1346–49 [Google Scholar]
  24. Pommier T, Canbäck B, Riemann L, Boström KH, Simu K. 24.  et al. 2007. Global patterns of diversity and community structure in marine bacterioplankton. Mol. Ecol. 16:867–80 [Google Scholar]
  25. Fuhrman JA, Steele JA, Hewson I, Schwalbach MS, Brown MV. 25.  et al. 2008. A latitudinal diversity gradient in planktonic marine bacteria. PNAS 105:7774–78 [Google Scholar]
  26. Martiny JBH, Bohannan BJM, Brown JH, Colwell RK, Fuhrman JA. 26.  et al. 2006. Microbial biogeography: putting microorganisms on the map. Nat. Rev. Microbiol. 4:102–12 [Google Scholar]
  27. De Wit R, Bouvier T. 27.  2006. “Everything is everywhere, but, the environment selects”; what did Baas Becking and Beijerinck really say? Environ. Microbiol. 8:755–58 [Google Scholar]
  28. Logue JB, Mouquet N, Peter H, Hillebrand H. 28.  Metacommunity Working Group 2011. Empirical approaches to metacommunities: a review and comparison with theory. Trends Ecol. Evol. 26:482–91 [Google Scholar]
  29. Bie T, Meester L, Brendonck L, Martens K, Goddeeris B. 29.  et al. 2012. Body size and dispersal mode as key traits determining metacommunity structure of aquatic organisms. Ecol. Lett. 15:740–47 [Google Scholar]
  30. Moritz C, Meynard CN, Devictor V, Guizien K, Labrune C. 30.  et al. 2013. Disentangling the role of connectivity, environmental filtering, and spatial structure on metacommunity dynamics. Oikos 122:1401–10 [Google Scholar]
  31. Barberán A, Casamayor EO, Fierer N. 31.  2014. The microbial contribution to macroecology. Front. Microbiol. 5:203 [Google Scholar]
  32. Leibold MA, Norberg J. 32.  2004. Biodiversity in metacommunities: plankton as complex adaptive systems?. Limnol. Oceanogr. 49:1278–89 [Google Scholar]
  33. Barberán A, Casamayor EO. 33.  2010. Global phylogenetic community structure and β-diversity patterns in surface bacterioplankton metacommunities. Aquat. Microb. Ecol. 59:1–10 [Google Scholar]
  34. Davies KF, Holyoak M, Preston KA, Offeman VA, Lum Q. 34.  2009. Factors controlling community structure in heterogeneous metacommunities. J. Anim. Ecology 78:937–44 [Google Scholar]
  35. Langenheder S, Székely AJ. 35.  2011. Species sorting and neutral processes are both important during the initial assembly of bacterial communities. ISME J 5:1086–94 [Google Scholar]
  36. Sul WJ, Oliver TA, Ducklow HW, Amaral-Zettler LA, Sogin ML. 36.  2013. Marine bacteria exhibit a bipolar distribution. PNAS 110:2342–47 [Google Scholar]
  37. Kellogg CA, Griffin DW. 37.  2006. Aerobiology and the global transport of desert dust. Trends Ecol. Evol. 21:638–44 [Google Scholar]
  38. Aller JY, Kuznetsova MR, Jahns CJ, Kemp PF. 38.  2005. The sea surface microlayer as a source of viral and bacterial enrichment in marine aerosols. J. Aerosol Sci. 36:801–12 [Google Scholar]
  39. Grossart H-P, Dziallas C, Leunert F, Tang KW. 39.  2010. Bacteria dispersal by hitchhiking on zooplankton. PNAS 107:11959–64 [Google Scholar]
  40. Lawrence JE, Suttle CA. 40.  2004. Effect of viral infection on sinking rates of Heterosigma akashiwo and its implications for bloom termination. Aquat. Microb. Ecol. 37:1–7 [Google Scholar]
  41. Turner JT. 41.  2002. Zooplankton fecal pellets, marine snow and sinking phytoplankton blooms. Aquat. Microb. Ecol. 27:57–102 [Google Scholar]
  42. Frada MJ, Schatz D, Farstey V, Ossolinski JE, Sabanay H. 42.  et al. 2014. Zooplankton may serve as transmission vectors for viruses infecting algal blooms in the ocean. Curr. Biol. 24:2592–97 [Google Scholar]
  43. Wilkins D, van Sebille E, Rintoul SR, Lauro FM, Cavicchioli R. 43.  2013. Advection shapes Southern Ocean microbial assemblages independent of distance and environment effects. Nat. Commun. 4:2457 [Google Scholar]
  44. Suttle CA, Chan AM. 44.  1994. Dynamics and distribution of cyanophages and their effect on marine Synechococcus spp. Appl. Environ. Microbiol. 60:3167–74 [Google Scholar]
  45. Wilhelm SW, Jeffrey WH, Dean AL, Meador J, Pakulski JD, Mitchell DL. 45.  2003. UV radiation induced DNA damage in marine viruses along a latitudinal gradient in the southeastern Pacific Ocean. Aquat. Microb. Ecol. 31:1–8 [Google Scholar]
  46. Weinbauer MG, Wilhelm SW, Suttle CA, Garza DR. 46.  1997. Photoreactivation compensates for UV damage and restores infectivity to natural marine virus communities. Appl. Environ. Microbiol. 63:2200–5 [Google Scholar]
  47. Jacquet S, Bratbak G. 47.  2003. Effects of ultraviolet radiation on marine virus-phytoplankton interactions. FEMS Microbiol. Ecol. 44:279–89 [Google Scholar]
  48. Garza DR, Suttle CA. 48.  1998. The effect of cyanophages on the mortality of Synechococcus spp. and selection for UV resistant viral communities. Microb. Ecol. 36:281–92 [Google Scholar]
  49. Weinbauer MG, Brettar I, Höfle MG. 49.  2003. Lysogeny and virus-induced mortality of bacterioplankton in surface, deep, and anoxic marine waters. Limnol. Oceanogr. 48:1457–65 [Google Scholar]
  50. Evans C, Brussaard CPD. 50.  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 [Google Scholar]
  51. Payet JP, Suttle CA. 51.  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 [Google Scholar]
  52. Wommack KE, Colwell RR. 52.  2000. Virioplankton: viruses in aquatic ecosystems. Microbiol. Mol. Biol. Rev. 64:69–114 [Google Scholar]
  53. Motegi C, Kaiser K, Benner R, Weinbauer MG. 53.  2015. Effect of P-limitation on prokaryotic and viral production in surface waters of the Northwestern Mediterranean Sea. J. Plankton Res. 37:16–20 [Google Scholar]
  54. Parada V, Herndl GJ, Weinbauer MG. 54.  2006. Viral burst size of heterotrophic prokaryotes in aquatic systems. J. Mar. Biol. Assoc. 86:613–21 [Google Scholar]
  55. Kang I, Oh HM, Kang D, Cho JC. 55.  2013. Genome of a SAR116 bacteriophage shows the prevalence of this phage type in the oceans. PNAS 110:12343–48 [Google Scholar]
  56. Zhao Y, Temperton B, Thrash JC, Schwalbach MS, Vergin KL. 56.  et al. 2013. Abundant SAR11 viruses in the ocean. Nature 494:357–60 [Google Scholar]
  57. Wilson WH, Carr NG, Mann NH. 57.  1996. The effect of phosphate status on the kinetics of cyanophage infection in the oceanic cyanobacterium Synechococcus sp. WH7803. J. Phycol. 32:506–16 [Google Scholar]
  58. Traving SJ, Clokie MRJ, Middelboe M. 58.  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 [Google Scholar]
  59. Short SM. 59.  2012. The ecology of viruses that infect eukaryotic algae. Environ. Microbiol. 14:2253–71 [Google Scholar]
  60. Lindell D, Jaffe JD, Johnson ZI, Church GM, Chisholm SW. 60.  2005. Photosynthesis genes in marine viruses yield proteins during host infection. Nature 438:86–89 [Google Scholar]
  61. Ignacio-Espinoza JC, Sullivan MB. 61.  2012. Phylogenomics of T4 cyanophages: lateral gene transfer in the “core” and origins of host genes. Environ. Microbiol. 14:2113–26 [Google Scholar]
  62. Labrie SJ, Frois-Moniz K, Osburne MS, Kelly L, Roggensack SE. 62.  et al. 2013. Genomes of marine cyanopodoviruses reveal multiple origins of diversity. Environ. Microbiol. 15:1356–76 [Google Scholar]
  63. Monier A, Welsh RM, Gentemann C, Weinstock G, Sodergren E. 63.  et al. 2012. Phosphate transporters in marine phytoplankton and their viruses: cross-domain commonalities in viral-host gene exchanges. Environ. Microbiol. 14:162–76 [Google Scholar]
  64. Fischer MG, Allen MJ, Wilson WH, Suttle CA. 64.  2010. Giant virus with a remarkable complement of genes infects marine zooplankton. PNAS 107:19508–13 [Google Scholar]
  65. Weynberg KD, Allen MJ, Gilg IC, Scanlan DJ, Wilson WH. 65.  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 [Google Scholar]
  66. Hellweger FL. 66.  2009. Carrying photosynthesis genes increases ecological fitness of cyanophage in silico. Environ. Microbiol. 11:1386–94 [Google Scholar]
  67. Waterbury JB, Valois FW. 67.  1993. Resistance to co-occurring phages enables marine Synechococcus communities to coexist with cyanophages abundant in seawater. Appl. Environ. Microbiol. 59:3393–99 [Google Scholar]
  68. Sullivan MB, Waterbury JB, Chisholm SW. 68.  2003. Cyanophages infecting the oceanic cyanobacterium Prochlorococcus. Nature 424:1047–51 [Google Scholar]
  69. Suttle CA, Chan AM. 69.  1993. Marine cyanophages infecting oceanic and coastal strains of Synechococcus: abundance, morphology, cross-infectivity and growth characteristics. Mar. Ecol. Prog. Ser. 92:99–109 [Google Scholar]
  70. Marston MF, Taylor S, Sme N, Parsons RJ, Noyes TJE, Martiny JBH. 70.  2013. Marine cyanophages exhibit local and regional biogeography. FEMS Microbiol. Rev. 15:1452–63 [Google Scholar]
  71. Cottrell MT, Suttle CA. 71.  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 [Google Scholar]
  72. Tai V, Lawrence JE, Lang AS, Chan AM, Culley AI, Suttle CA. 72.  2003. Characterization of HaRNAV, a single-stranded RNA virus causing lysis of Heterosigma akashiwo (Raphidophyceae). J. Phycol. 39:343–52 [Google Scholar]
  73. Tomaru Y, Katanozaka N, Nishida K, Shirai Y, Tarutani K. 73.  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 [Google Scholar]
  74. Clerissi C, Desdevises Y, Grimsley N. 74.  2012. Prasinoviruses of the marine green alga Ostreococcus tauri are mainly species specific. J. Virol. 86:4611–19 [Google Scholar]
  75. Derelle E, Monier A, Cooke R, Worden AZ, Grimsley NH, Moreau H. 75.  2015. Diversity of viruses infecting the green micro-alga Ostreococcus lucimarinus. J. Virol. 89:5812–21 [Google Scholar]
  76. Holmfeldt K, Middelboe M, Nybroe O, Riemann L. 76.  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 [Google Scholar]
  77. Nemergut DR, Costello EK, Hamady M, Lozupone C, Jiang L. 77.  et al. 2011. Global patterns in the biogeography of bacterial taxa. Environ. Microbiol. 13:135–44 [Google Scholar]
  78. Bergh Ø, Børsheim KY, Bratbak G, Heldal M. 78.  1989. High abundance of viruses found in aquatic environments. Nature 340:467–68 [Google Scholar]
  79. Proctor LM, Fuhrman JA. 79.  1990. Viral mortality of marine bacteria and cyanobacteria. Nature 343:60–62 [Google Scholar]
  80. Parsons RJ, Breitbart M, Lomas MW, Carlson CA. 80.  2012. Ocean time-series reveals recurring seasonal patterns of virioplankton dynamics in the northwestern Sargasso Sea. ISME J 6:273–84 [Google Scholar]
  81. Johannessen TV, Bratbak G, Larsen A, Ogata H, Egge ES. 81.  et al. 2015. Characterisation of three novel giant viruses reveals huge diversity among viruses infecting Prymnesiales (Haptophyta). Virology 476:180–88 [Google Scholar]
  82. Huang S, Wang K, Jiao N, Chen F. 82.  2012. Genome sequences of siphoviruses infecting marine Synechococcus unveil a diverse cyanophage group and extensive phage-host genetic exchanges. Environ. Microbiol. 14:540–58 [Google Scholar]
  83. Holmfeldt K, Solonenko N, Shah M, Corrier K, Riemann L. 83.  et al. 2013. Twelve previously unknown phage genera are ubiquitous in global oceans. PNAS 110:12798–803 [Google Scholar]
  84. Mizuno CM, Rodriguez-Valera F, Kimes NE, Ghai R. 84.  2013. Expanding the marine virosphere using metagenomics. PLOS Genet. 9:e1003987 [Google Scholar]
  85. Labonté JM, Suttle CA. 85.  2013. Metagenomic and whole-genome analysis reveals new lineages of gokushoviruses and biogeographic separation in the sea. Front. Microbiol. 4:404 [Google Scholar]
  86. Adriaenssens EM, Cowan DA. 86.  2014. Using signature genes as tools to assess environmental viral ecology and diversity. Appl. Environ. Microbiol. 80:4470–80 [Google Scholar]
  87. Sullivan MB, Coleman ML, Quinlivan V, Rosenkrantz JE, DeFrancesco AS. 87.  et al. 2008. Portal protein diversity and phage ecology. Environ. Microbiol. 10:2810–23 [Google Scholar]
  88. Bellec L, Grimsley N, Moreau H, Desdevises Y. 88.  2009. Phylogenetic analysis of new Prasinoviruses (Phycodnaviridae) that infect the green unicellular algae Ostreococcus, Bathycoccus and Micromonas. Environ. Microbiol. Rep 1:114–23 [Google Scholar]
  89. Culley AI, Steward GF. 89.  2007. New genera of RNA viruses in subtropical seawater, inferred from polymerase gene sequences. Appl. Environ. Microbiol. 73:5937–44 [Google Scholar]
  90. Sakowski EG, Munsell EV, Hyatt M, Kress W, Williamson SJ. 90.  et al. 2014. Ribonucleotide reductases reveal novel viral diversity and predict biological and ecological features of unknown marine viruses. PNAS 111:15786–91 [Google Scholar]
  91. Schmidt HF, Sakowski EG, Williamson SJ, Polson SW, Wommack KE. 91.  2014. Shotgun metagenomics indicates novel family A DNA polymerases predominate within marine virioplankton. ISME J. 8:103–14 [Google Scholar]
  92. Hurwitz BL, Brum JR, Sullivan MB. 92.  2015. Depth-stratified functional and taxonomic niche specialization in the ‘core’ and ‘flexible’ Pacific Ocean Virome. ISME J. 9:472–84 [Google Scholar]
  93. Solonenko SA, Ignacio-Espinoza JC, Alberti A, Cruaud C, Hallam SJ. 93.  et al. 2013. Sequencing platform and library preparation choices impact viral metagenomes. BMC Genomics 14:320 [Google Scholar]
  94. Brum JR, Ignacio-Espinoza JC, Roux S, Doulcier G, Acinas SG. 94.  et al. 2015. Patterns and ecological drivers of ocean viral communities. Science 348:1261498 [Google Scholar]
  95. Hurwitz BL, Westveld AH, Brum JR, Sullivan MB. 95.  2014. Modeling ecological drivers in marine viral communities using comparative metagenomics and network analyses. PNAS 111:10714–19 [Google Scholar]
  96. Hurwitz BL, Sullivan MB. 96.  2013. The Pacific Ocean Virome (POV): a marine viral metagenomic dataset and associated protein clusters for quantitative viral ecology. PLOS ONE 8:e57355 [Google Scholar]
  97. Needham DM, Chow C-ET, Cram JA, Sachdeva R, Parada A, Fuhrman JA. 97.  2013. Short-term observations of marine bacterial and viral communities: patterns, connections and resilience. ISME J. 7:1274–85 [Google Scholar]
  98. Chow C-ET, Kim DY, Sachdeva R, Caron DA, Fuhrman JA. 98.  2014. Top-down controls on bacterial community structure: microbial network analysis of bacteria, T4-like viruses and protists. ISME J. 8:816–29 [Google Scholar]
  99. Weitz JS, Poisot T, Meyer JR, Flores CO, Valverde S. 99.  et al. 2013. Phage-bacteria infection networks. Trends Microbiol. 21:82–91 [Google Scholar]
  100. Martinez JM, Schroeder DC, Larsen A, Bratbak G, Wilson WH. 100.  2007. Molecular dynamics of Emiliania huxleyi and cooccurring viruses during two separate mesocosm studies. Appl. Environ. Microbiol. 73:554–62 [Google Scholar]
  101. Tomaru Y, Tarutani K, Yamaguchi M, Nagasaki K. 101.  2004. Quantitative and qualitative impacts of viral infection on a Heterosigma akashiwo (Raphidophyceae) bloom in Hiroshima Bay, Japan. Aquat. Microb. Ecol. 34:227–38 [Google Scholar]
  102. Short SM, Suttle CA. 102.  2003. Temporal dynamics of natural communities of marine algal viruses and eukaryotes. Aquat. Microb. Ecol. 32:107–19 [Google Scholar]
  103. Holmfeldt K, Howard-Varona C, Solonenko N, Sullivan MB. 103.  2014. Contrasting genomic patterns and infection strategies of two co-existing Bacteroidetes podovirus genera. Environ. Microbiol. 16:2501–13 [Google Scholar]
  104. Deng L, Ignacio-Espinoza JC, Gregory AC, Poulos BT, Weitz JS. 104.  et al. 2014. Viral tagging reveals discrete populations in Synechococcus viral genome sequence space. Nature 513:242–45 [Google Scholar]
  105. Chow C-ET, Winget DM, White RA III, Hallam SJ, Suttle CA. 105.  2015. Combining genomic sequencing methods to explore viral diversity and reveal potential virus-host interactions. Front. Microbiol. 6:265 [Google Scholar]
  106. Martinez JM, Swan BK, Wilson WH. 106.  2014. Marine viruses, a genetic reservoir revealed by targeted viromics. ISME J. 8:1079–88 [Google Scholar]
  107. Roux S, Hawley AK, Torres Beltran M, Scofield M, Schwientek P. 107.  et al. 2014. Ecology and evolution of viruses infecting uncultivated SUP05 bacteria as revealed by single-cell- and meta-genomics. eLife 3:e03125 [Google Scholar]
  108. Labonté JM, Swan BK, Poulos B, Luo H, Koren S. 108.  et al. 2015. Single-cell genomics-based analysis of virus-host interactions in marine surface bacterioplankton. ISME J doi: 10.1038/ismej.2015.48 [Google Scholar]
  109. Breitbart M, Miyake JH, Rohwer F. 109.  2004. Global distribution of nearly identical phage-encoded DNA sequences. FEMS Microbiol. Lett. 236:249–56 [Google Scholar]
  110. Clasen JL, Hanson CA, Ibrahim Y, Weihe C. 110.  2013. Diversity and temporal dynamics of Southern California coastal marine cyanophage isolates. Aquat. Microb. Ecol. 69:17–31 [Google Scholar]
  111. Kang I, Cho J-C. 111.  2014. Depth-specific distribution of the SAR116 phages revealed by virome binning. J. Microbiol. Biotechnol. 24:592–96 [Google Scholar]
  112. Lindell D, Jaffe JD, Coleman ML, Futschik ME, Axmann IM. 112.  et al. 2007. Genome-wide expression dynamics of a marine virus and host reveal features of co-evolution. Nature 449:83–86 [Google Scholar]
  113. Thompson LR, Zeng Q, Kelly L, Huang KH, Singer AU. 113.  et al. 2011. Phage auxiliary metabolic genes and the redirection of cyanobacterial host carbon metabolism. PNAS 108:E757–64 [Google Scholar]
  114. Zwirglmaier K, Jardillier L, Ostrowski M, Mazard S, Garczarek L. 114.  et al. 2008. Global phylogeography of marine Synechococcus and Prochlorococcus reveals a distinct partitioning of lineages among oceanic biomes. Environ. Microbiol. 10:147–61 [Google Scholar]
  115. Malmstrom RR, Coe A, Kettler GC, Martiny AC, Frias-Lopez J. 115.  et al. 2010. Temporal dynamics of Prochlorococcus ecotypes in the Atlantic and Pacific oceans. ISME J. 4:1252–64 [Google Scholar]
  116. Martiny AC, Tai APK, Veneziano D, Primeau F, Chisholm SW. 116.  2009. Taxonomic resolution, ecotypes and the biogeography of Prochlorococcus. Environ. Microbiol. 11:823–32 [Google Scholar]
  117. Jameson E, Mann NH, Joint I, Sambles C, Mühling M. 117.  2011. The diversity of cyanomyovirus populations along a North-South Atlantic Ocean transect. ISME J. 5:1713–21 [Google Scholar]
  118. Wilson WH, Fuller NJ, Joint IR, Mann NH. 118.  1999. Analysis of cyanophage diversity and population structure in a south-north transect of the Atlantic Ocean. Bull. Inst. Oceanogr. Monaco 19:209–16 [Google Scholar]
  119. Green JL, Bohannan BJM, Whitaker RJ. 119.  2008. Microbial biogeography: from taxonomy to traits. Science 320:1039–43 [Google Scholar]
  120. Barton AD, Pershing AJ, Litchman E, Record NR, Edwards KF. 120.  et al. 2013. The biogeography of marine plankton traits. Ecol. Lett. 16:522–34 [Google Scholar]
  121. Sharon I, Battchikova N, Aro E-M, Giglione C, Meinnel T. 121.  et al. 2011. Comparative metagenomics of microbial traits within oceanic viral communities. ISME J. 5:1178–90 [Google Scholar]
  122. Sharon I, Tzahor S, Williamson SJ, Shmoish M, Man-Aharonovich D. 122.  et al. 2007. Viral photosynthetic reaction center genes and transcripts in the marine environment. ISME J. 1:492–501 [Google Scholar]
  123. Chenard C, Suttle CA. 123.  2008. Phylogenetic diversity of sequences of cyanophage photosynthetic gene psbA in marine and freshwaters. Appl. Environ. Microbiol. 74:5317–24 [Google Scholar]
  124. Verreydt D, De Meester L, Decaestecker E, Villena M-J, Van Der Gucht K. 124.  et al. 2012. Dispersal-mediated trophic interactions can generate apparent patterns of dispersal limitation in aquatic metacommunities. Ecol. Lett. 15:218–26 [Google Scholar]
  125. Williamson SJ, Rusch DB, Yooseph S, Halpern AL, Heidelberg KB. 125.  et al. 2008. The Sorcerer II Global Ocean Sampling Expedition: metagenomic characterization of viruses within aquatic microbial samples. PLOS ONE 3e1456 [Google Scholar]
  126. Huang S, Zhang S, Jiao N, Chen F. 126.  2015. Marine cyanophages demonstrate biogeographic patterns throughout the global ocean. Appl. Environ. Microbiol. 81:441–52 [Google Scholar]
  127. Roux S, Tournayre J, Mahul A, Debroas D, Enault F. 127.  2014. Metavir 2: new tools for viral metagenome comparison and assembled virome analysis. BMC Bioinform. 15:76 [Google Scholar]
  128. Dinsdale EA, Pantos O, Smriga S, Edwards RA, Angly FE. 128.  et al. 2008. Microbial ecology of four coral atolls in the Northern Line Islands. PLOS ONE 3:e1584 [Google Scholar]
  129. Williamson SJ, Allen LZ, Lorenzi HA, Fadrosh DW, Brami D. 129.  et al. 2012. Metagenomic exploration of viruses throughout the Indian Ocean. PLOS ONE 7:e42047 [Google Scholar]
  130. Cassman N, Prieto-Davó A, Walsh K, Silva GGZ, Angly FE. 130.  et al. 2012. Oxygen minimum zones harbour novel viral communities with low diversity. Environ. Microbiol. 14:3043–65 [Google Scholar]
  131. Sullivan MB, Coleman ML, Weigele P, Rohwer F, Chisholm SW. 131.  2005. Three Prochlorococcus cyanophage genomes: signature features and ecological interpretations. PLOS Biol. 3:790–806 [Google Scholar]
  132. Follows MJ, Dutkiewicz S, Grant S, Chisholm SW. 132.  2007. Emergent biogeography of microbial communities in a model ocean. Science 315:1843–46 [Google Scholar]
  133. Monier A, Comte J, Babin M, Forest A, Matsuoka A, Lovejoy C. 133.  2015. Oceanographic structure drives the assembly processes of microbial eukaryotic communities. ISME J 9:990–1002 [Google Scholar]
  134. Rodríguez-Ramos T, Marañón E, Cermeño P. 134.  2015. Marine nano- and microphytoplankton diversity: redrawing global patterns from sampling-standardized data. Glob. Ecol. Biogeogr. 24:527–38 [Google Scholar]
  135. Monier A, Claverie J-MM, Ogata H. 135.  2008. Taxonomic distribution of large DNA viruses in the sea. Genome Biol 9:R106 [Google Scholar]
  136. Bellec L, Clerissi C, Edern R, Foulon E, Simon N. 136.  et al. 2014. Cophylogenetic interactions between marine viruses and eukaryotic picophytoplankton. BMC Evol. Biol. 14:59 [Google Scholar]
  137. Derelle E, Ferraz C, Escande M-L, Eychenié S, Cooke R. 137.  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 [Google Scholar]
  138. Waters RE, Chan AT. 138.  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 [Google Scholar]
  139. Clerissi C, Grimsley N, Ogata H, Hingamp P, Poulain J, Desdevises Y. 139.  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 [Google Scholar]
  140. Clerissi C, Grimsley N, Subirana L, Maria E, Oriol L. 140.  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 [Google Scholar]
  141. Steward GF, Culley AI, Mueller JA, Wood-Charlson EM, Belcaid M, Poisson G. 141.  2013. Are we missing half of the viruses in the ocean?. ISME J. 7:672–79 [Google Scholar]
  142. Lang AS, Rise ML, Culley AI, Steward GF. 142.  2009. RNA viruses in the sea. FEMS Microbiol. Rev. 33:295–323 [Google Scholar]
  143. Nagasaki K, Tomaru Y, Katanozaka N, Shirai Y, Nishida K. 143.  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 [Google Scholar]
  144. Shirai Y, Tomaru Y, Takao Y, Suzuki H, Nagumo T, Nagasaki K. 144.  2008. Isolation and characterization of a single-stranded RNA virus infecting the marine planktonic diatom Chaetoceros tenuissimus Meunier. Appl. Environ. Microbiol. 74:4022–27 [Google Scholar]
  145. Tomaru Y, Hata N, Masuda T, Tsuji M, Igata K. 145.  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 [Google Scholar]
  146. Attoui H, Jaafar FM, Belhouchet M, de Micco P, de Lamballerie X, Brussaard CPD. 146.  2006. Micromonas pusilla reovirus: a new member of the family Reoviridae assigned to a novel proposed genus (Mimoreovirus). J. Gen. Virol. 87:1375–83 [Google Scholar]
  147. Culley AI, Lang AS, Suttle CA. 147.  2006. Metagenomic analysis of coastal RNA virus communities. Science 312:1795–98 [Google Scholar]
  148. Rosario K, Duffy S, Breitbart M. 148.  2009. Diverse circovirus-like genome architectures revealed by environmental metagenomics. J. Gen. Virol. 90:2418–24 [Google Scholar]
  149. Tucker KP, Parsons R, Symonds EM, Breitbart M. 149.  2010. Diversity and distribution of single-stranded DNA phages in the North Atlantic Ocean. ISME J. 5:822–30 [Google Scholar]
  150. Roux S, Krupovic M, Poulet A, Debroas D, Enault F. 150.  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 [Google Scholar]
  151. Labonté JM, Suttle CA. 151.  2013. Previously unknown and highly divergent ssDNA viruses populate the oceans. ISME J 7:2169–77 [Google Scholar]
  152. Labonté JM, Hallam SJ, Suttle CA. 152.  2015. Previously unknown evolutionary groups dominate the ssDNA gokushoviruses in oxic and anoxic waters of a coastal marine environment. Front. Microbiol. 6:315 [Google Scholar]
  153. Krupovic M, Forterre P. 153.  2015. Single-stranded DNA viruses employ a variety of mechanisms for integration into host genomes. Ann. N.Y. Acad. Sci. 1341:41–53 [Google Scholar]
  154. Thingstad TF, Vage S, Storesund JE, Sandaa R-A, Giske J. 154.  2014. A theoretical analysis of how strain-specific viruses can control microbial species diversity. PNAS 111:7813–18 [Google Scholar]

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