Phage puppet masters of the marine microbial realm

Abstract

Viruses numerically dominate our oceans; however, we have only just begun to document the diversity, host range and infection dynamics of marine viruses, as well as the subsequent effects of infection on both host cell metabolism and oceanic biogeochemistry. Bacteriophages (that is, phages: viruses that infect bacteria) are highly abundant and are known to play critical roles in bacterial mortality, biogeochemical cycling and horizontal gene transfer. This Review Article summarizes current knowledge of marine viral ecology and highlights the importance of phage particles to the dissolved organic matter pool, as well as the complex interactions between phages and their bacterial hosts. We emphasize the newly recognized roles of phages as puppet masters of their bacterial hosts, where phages are capable of altering the metabolism of infected bacteria through the expression of auxiliary metabolic genes and the redirection of host gene expression patterns. Finally, we propose the ‘royal family model’ as a hypothesis to describe successional patterns of bacteria and phages over time in marine systems, where despite high richness and significant seasonal differences, only a small number of phages appear to continually dominate a given marine ecosystem. Although further testing is required, this model provides a framework for assessing the specificity and ecological consequences of phage–host dynamics.

Access options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

All prices are NET prices.

Fig. 1: The size of biology in the oceans spans nine orders of magnitude from the smallest viruses (~17 nm) to the largest charismatic megafauna (blue whale, ~33 m).
Fig. 2: Spatial heterogeneity in the abundance of bacteria and VLPs may exist on extremely small scales in the oceans.
Fig. 3: The two main lifestyles of marine phages: lytic versus lysogenic.
Fig. 4: The marine food web, emphasizing the central role of the microbial loop and viral shunt in recycling DOM.
Fig. 5: Venn diagram showing cyanobacterial (left) and sulfur-oxidizing (right) cells.

References

  1. 1.

    Wommack, K. & Colwell, R. Virioplankton: viruses in aquatic ecosystems. Microbiol. Mol. Biol. Rev. 64, 69–114 (2000).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  2. 2.

    Suttle, C. Marine viruses — major players in the global ecosystem. Nat. Rev. Microbiol. 5, 801–812 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. 3.

    Brum, J. R., Schenck, R. O. & Sullivan, M. B. Global morphological analysis of marine viruses shows minimal regional variation and dominance of non-tailed viruses. ISME J. 7, 1738–1751 (2013).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  4. 4.

    Blatner, D. Spectrums: Our Mind-Boggling Universe from Infinitesimal to Infinity (Bloomsbury Publishing, London, 2012).

    Google Scholar 

  5. 5.

    Munn, C. Viruses as pathogens of marine organisms—from bacteria to whales. JMBA 86, 453–467 (2006).

    Google Scholar 

  6. 6.

    Spencer, R. A marine bacteriophage. Nature 175, 690–691 (1955).

    Article  CAS  PubMed  Google Scholar 

  7. 7.

    Bergh, Ø., Børsheim, K. Y., Bratbak, G. & Heldal, M. High abundance of viruses found in aquatic environments. Nature 340, 467–468 (1989).

    Article  CAS  PubMed  Google Scholar 

  8. 8.

    Proctor, L. & Fuhrman, J. Viral mortality of marine bacteria and cyanobacteria. Nature 343, 60–62 (1990).

    Article  Google Scholar 

  9. 9.

    Suttle, C. & Fuhrman, J. in Manual of Aquatic Viral Ecology (eds Wilhelm, S. W. et al.) Ch. 15, 145–153 (American Society of Limnology and Oceanography, 2010).

  10. 10.

    Biller, S. J. et al. Membrane vesicles in sea water: heterogeneous DNA content and implications for viral abundance estimates. ISME J. 11, 394–404 (2017).

    Article  CAS  PubMed  Google Scholar 

  11. 11.

    Tomaru, Y. & Nagasaki, K. Flow cytometric detection and enumeration of DNA and RNA viruses infecting marine eukaryotic microalgae. J. Oceanogr. 63, 215–221 (2007).

    Article  CAS  Google Scholar 

  12. 12.

    Forterre, P., Soler, N., Krupovic, M., Marguet, E. & Ackermann, H.-W. Fake virus particles generated by fluorescence microscopy. Trends Microbiol. 21, 1–5 (2013).

    Article  CAS  PubMed  Google Scholar 

  13. 13.

    Parsons, R., Breitbart, M., Lomas, M. & Carlson, C. Ocean time-series reveals recurring seasonal patterns of virioplankton dynamics in the northwestern Sargasso Sea. ISME J. 6, 273–284 (2012).

    Article  CAS  PubMed  Google Scholar 

  14. 14.

    Wigington, C. H. et al. Re-examination of the relationship between marine virus and microbial cell abundances. Nat. Microbiol. 1, 15024 (2016).

    Article  CAS  PubMed  Google Scholar 

  15. 15.

    Parikka, K. J., Le Romancer, M., Wauters, N. & Jacquet, S. Deciphering the virus‐to‐prokaryote ratio (VPR): insights into virus–host relationships in a variety of ecosystems. Biol. Rev. 92, 1081–1100 (2017).

    Article  PubMed  Google Scholar 

  16. 16.

    Knowles, B. et al. Lytic to temperate switching of viral communities. Nature 531, 466–470 (2016).

    Article  CAS  PubMed  Google Scholar 

  17. 17.

    Sullivan, M. B., Weitz, J. S. & Wilhelm, S. Viral ecology comes of age. Environ. Microbiol. Rep. 9, 33–35 (2017).

    Article  PubMed  Google Scholar 

  18. 18.

    Azam, F. Microbial control of oceanic carbon flux: the plot thickens. Science 280, 694–696 (1998).

    Article  CAS  Google Scholar 

  19. 19.

    Carreira, C., Larsen, M., Glud, R. N., Brussaard, C. P. & Middelboe, M. Heterogeneous distribution of prokaryotes and viruses at the microscale in a tidal sediment. Aquat. Microb. Ecol. 69, 183–192 (2013).

    Article  Google Scholar 

  20. 20.

    Seymour, J., Seuront, L., Doubell, M., Waters, R. & Mitchell, J. Microscale patchiness of virioplankton. JMBA 86, 551–561 (2006).

    Google Scholar 

  21. 21.

    Dann, L. M. et al. Virio- and bacterioplankton microscale distributions at the sediment-water interface. PLoS ONE 9, e102805 (2014).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  22. 22.

    Dann, L. M., Paterson, J. S., Newton, K., Oliver, R. & Mitchell, J. G. Distributions of virus-like particles and prokaryotes within microenvironments. PLoS ONE 11, e0146984 (2016).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  23. 23.

    Long, R. & Azam, F. Microscale patchiness of bacterioplankton assemblage richness in seawater. Aquat. Microbiol. Ecol. 26, 103–113 (2001).

    Article  Google Scholar 

  24. 24.

    Parada, V., Herndl, G. J. & Weinbauer, M. G. Viral burst size of heterotrophic prokaryotes in aquatic systems. JMBA 86, 613–621 (2006).

    Google Scholar 

  25. 25.

    Howard-Varona, C., Hargreaves, K. R., Abedon, S. T. & Sullivan, M. B. Lysogeny in nature: mechanisms, impact and ecology of temperate phages. ISME J. 11, 1511–1520 (2017).

    PubMed  PubMed Central  Article  Google Scholar 

  26. 26.

    Oppenheim, A. B., Kobiler, O., Stavans, J., Court, D. L. & Adhya, S. Switches in bacteriophage lambda development. Annu. Rev. Genet. 39, 409–429 (2005).

    Article  CAS  PubMed  Google Scholar 

  27. 27.

    Paul, J. Prophages in marine bacteria: dangerous molecular time bombs or the key to survival in the seas? ISME J. 2, 579–589 (2008).

    Article  CAS  PubMed  Google Scholar 

  28. 28.

    Trinh, J. T., Székely, T., Shao, Q., Balázsi, G. & Zeng, L. Cell fate decisions emerge as phages cooperate or compete inside their host. Nat. Commun. 8, 14341 (2017).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  29. 29.

    Erez, Z. et al. Communication between viruses guides lysis–lysogeny decisions. Nature 541, 488–493 (2017).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  30. 30.

    Jiang, S. C. & Paul, J. H. Seasonal and diel abundance of viruses and occurrence of lysogeny/bacteriocinogeny in the marine environment. Mar. Ecol. Prog. Ser. 104, 163–172 (1994).

    Article  Google Scholar 

  31. 31.

    Cochran, P. K., Kellogg, C. A. & Paul, J. H. Prophage induction of indigenous marine lysogenic bacteria by environmental pollutants. Mar. Ecol. Prog. Ser. 164, 125–133 (1998).

    Article  CAS  Google Scholar 

  32. 32.

    McDaniel, L., Houchin, L., Williamson, S. & Paul, J. Lysogeny in marine Synechococcus. Nature 415, 496 (2002).

    Article  CAS  PubMed  Google Scholar 

  33. 33.

    Knowles, B. et al. Variability and host density independence in inductions-based estimates of environmental lysogeny. Nat. Microbiol. 2, 17064 (2017).

    Article  CAS  PubMed  Google Scholar 

  34. 34.

    Akhter, S., Aziz, R. K. & Edwards, R. A. PhiSpy: a novel algorithm for finding prophages in bacterial genomes that combines similarity-and composition-based strategies. Nucleic Acids Res. 40, e126 (2012).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  35. 35.

    Weitz, J. S., Beckett, S. J., Brum, J. R., Cael, B. & Dushoff, J. Lysis, lysogeny and virus–microbe ratios. Nature 549, E1–E3 (2017).

    Article  CAS  PubMed  Google Scholar 

  36. 36.

    Brum, J. R., Hurwitz, B. L., Schofield, O., Ducklow, H. W. & Sullivan, M. B. Seasonal time bombs: dominant temperate viruses affect Southern Ocean microbial dynamics. ISME J. 10, 437–449 (2016).

    Article  CAS  PubMed  Google Scholar 

  37. 37.

    McDaniel, L. D., Rosario, K., Breitbart, M. & Paul, J. H. Comparative metagenomics: natural populations of induced prophages demonstrate highly unique, lower diversity viral sequences. Environ. Microbiol. 16, 570–585 (2014).

    Article  CAS  PubMed  Google Scholar 

  38. 38.

    Pomeroy, L. R., Williams, P. JleB., Azam, F. & Hobbie, J. E. The microbial loop. Oceanography 20, 28–33 (2007).

    Article  Google Scholar 

  39. 39.

    Whitman, W., Coleman, D. & Wiebe, W. Prokaryotes: the unseen majority. Proc. Natl Acad. Sci. USA 95, 6578–6583 (1998).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  40. 40.

    Azam, F. et al. The ecological role of water-column microbes in the sea. Mar. Ecol. Prog. Ser. 10, 257–263 (1983).

    Article  Google Scholar 

  41. 41.

    Ducklow, H. W., Steinberg, D. K. & Buesseler, K. O. Upper ocean carbon export and the biological pump. Oceanography 14, 50–58 (2001).

    Article  Google Scholar 

  42. 42.

    Wilhelm, S. W. & Suttle, C. A. Viruses and nutrient cycles in the sea. BioScience 49, 781–783 (1999).

    Article  Google Scholar 

  43. 43.

    Fuhrman, J. Marine viruses and their biogeochemical and ecological effects. Nature 399, 541–548 (1999).

    Article  CAS  PubMed  Google Scholar 

  44. 44.

    Weinbauer, M. Ecology of prokaryotic viruses. FEMS Microbiol. Rev. 28, 127–181 (2004).

    Article  CAS  PubMed  Google Scholar 

  45. 45.

    Laber, C. P. et al. Coccolithovirus facilitation of carbon export in the North Atlantic. Nat. Microbiol. 1, 537–547 (2018).

    Article  CAS  Google Scholar 

  46. 46.

    Guidi, L. et al. Plankton networks driving carbon export in the oligotrophic ocean. Nature 532, 465 (2016).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  47. 47.

    Weitz, J. S. et al. A multitrophic model to quantify the effects of marine viruses on microbial food webs and ecosystem processes. ISME J. 9, 1352–1364 (2015).

    PubMed  PubMed Central  Article  Google Scholar 

  48. 48.

    Jover, L. F., Effler, T. C., Buchan, A., Wilhelm, S. W. & Weitz, J. S. The elemental composition of virus particles: implications for marine biogeochemical cycles. Nat. Rev. Microbiol. 12, 519–528 (2014).

    Article  CAS  PubMed  Google Scholar 

  49. 49.

    Bonnain, C., Breitbart, M. & Buck, K. N. The ferrojan horse hypothesis: Iron-virus interactions in the ocean. Front. Mar. Sci. 3, 82 (2016).

    Article  Google Scholar 

  50. 50.

    Breitbart, M., Thompson, L., Suttle, C. & Sullivan, M. Exploring the vast diversity of marine viruses. Oceanography 20, 135–139 (2007).

    Article  Google Scholar 

  51. 51.

    Casjens, S. R. & Hendrix, R. W. Bacteriophage lambda: early pioneer and still relevant. Virology 479, 310–330 (2015).

    Article  CAS  PubMed  Google Scholar 

  52. 52.

    Rohwer, F. et al. The complete genomic sequence of the marine phage Roseophage SIO1 shares homology with non-marine phages. Limnol. Oceanogr. 42, 408–418 (2000).

    Article  Google Scholar 

  53. 53.

    Lindell, D. et al. Photosynthesis genes in Prochlorococcus cyanophage. Proc. Natl Acad. Sci. USA 101, 11013–11018 (2004).

    Article  CAS  PubMed  Google Scholar 

  54. 54.

    Mann, N., Cook, A., Millard, A., Bailey, S. & Clokie, M. Marine ecosystems: bacterial photosynthesis genes in a virus. Nature 424, 741 (2003).

    Article  CAS  PubMed  Google Scholar 

  55. 55.

    Hurwitz, B. L., Hallam, S. J. & Sullivan, M. B. Metabolic reprogramming by viruses in the sunlit and dark ocean. Genome Biol. 14, R123 (2013).

    PubMed  PubMed Central  Article  Google Scholar 

  56. 56.

    Sharon, I. et al. Comparative metagenomics of microbial traits within oceanic viral communities. ISME J. 5, 1178–1190 (2011).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  57. 57.

    Roux, S. et al. Ecogenomics and potential biogeochemical impacts of globally abundant ocean viruses. Nature 537, 689–693 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. 58.

    Hurwitz, B. L., Brum, J. R. & Sullivan, M. B. Depth-stratified functional and taxonomic niche specialization in the ‘core’ and ‘flexible’ Pacific Ocean virome. ISME J. 9, 472–484 (2015).

    Article  CAS  PubMed  Google Scholar 

  59. 59.

    Puxty, R. J., Millard, A. D., Evans, D. J. & Scanlan, D. J. Shedding new light on viral photosynthesis. Photosynth. Res. 126, 71–97 (2015).

    Article  CAS  PubMed  Google Scholar 

  60. 60.

    Crummett, L. T., Puxty, R. J., Weihe, C., Marston, M. F. & Martiny, J. B. The genomic content and context of auxiliary metabolic genes in marine cyanomyoviruses. Virology 499, 219–229 (2016).

    Article  CAS  PubMed  Google Scholar 

  61. 61.

    Gao, E.-B., Huang, Y. & Ning, D. Metabolic genes within cyanophage genomes: implications for diversity and evolution. Genes 7, 80 (2016).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  62. 62.

    Enav, H., Mandel-Gutfreund, Y. & Béjà, O. Comparative metagenomic analyses reveal viral-induced shifts of host metabolism towards nucleotide biosynthesis. Microbiome 2, 9 (2014).

    PubMed  PubMed Central  Article  Google Scholar 

  63. 63.

    Bryan, M. et al. Evidence for the intense exchange of MazG in marine cyanophages by horizontal gene transfer. PLoS ONE 3, e2048 (2008).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  64. 64.

    Williamson, S. et al. The Sorcerer II global ocean sampling expedition: metagenomic characterization of viruses within aquatic microbial samples. PLoS ONE 3, e1456 (2008).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  65. 65.

    Kelly, L., Ding, H., Huang, K. H., Osburne, M. S. & Chisholm, S. W. Genetic diversity in cultured and wild marine cyanomyoviruses reveals phosphorus stress as a strong selective agent. ISME J. 7, 1827–1841 (2013).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  66. 66.

    Zeng, Q. & Chisholm, S. W. Marine viruses exploit their host’s two-component regulatory system in response to resource limitation. Curr. Biol. 22, 124–128 (2012).

    Article  CAS  PubMed  Google Scholar 

  67. 67.

    Lin, X., Ding, H. & Zeng, Q. Transcriptomic response during phage infection of a marine cyanobacterium under phosphorus‐limited conditions. Environ. Microbiol. 18, 450–460 (2016).

    Article  CAS  PubMed  Google Scholar 

  68. 68.

    Lindell, D., Jaffe, J., Johnson, Z., Church, G. & Chisholm, S. Photosynthesis genes in marine viruses yield proteins during host infection. Nature 438, 86–89 (2005).

    Article  CAS  PubMed  Google Scholar 

  69. 69.

    Hurwitz, B. L. & U’Ren, J. M. Viral metabolic reprogramming in marine ecosystems. Curr. Opin. Microbiol. 31, 161–168 (2016).

    Article  CAS  PubMed  Google Scholar 

  70. 70.

    Holmfeldt, K. et al. Twelve previously unknown phage genera are ubiquitous in global oceans. Proc. Natl Acad. Sci. USA 110, 12798–12803 (2013).

    Article  PubMed  Google Scholar 

  71. 71.

    Roux, S., Enault, F., Ravet, V., Pereira, O. & Sullivan, M. B. Genomic characteristics and environmental distributions of the uncultivated Far-T4 phages. Front. Microbiol. 6, 199 (2015).

    PubMed  PubMed Central  Google Scholar 

  72. 72.

    Sabri, M. et al. Genome annotation and intraviral interactome for the Streptococcus pneumoniae virulent phage Dp-1. J. Bacteriol. 193, 551–562 (2011).

    Article  CAS  PubMed  Google Scholar 

  73. 73.

    Frank, J. A. et al. Structure and function of a cyanophage-encoded peptide deformylase. ISME J. 7, 1150–1160 (2013).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  74. 74.

    Dammeyer, T., Bagby, S., Sullivan, M., Chisholm, S. & Frankenberg-Dinkel, N. Efficient phage-mediated pigment biosynthesis in oceanic cyanobacteria. Curr. Biol. 18, 442–448 (2008).

    Article  CAS  PubMed  Google Scholar 

  75. 75.

    Rappoport, N. & Linial, M. Viral proteins acquired from a host converge to simplified domain architectures. PLoS Comput. Biol. 8, e1002364 (2012).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  76. 76.

    Thompson, L. R. et al. Phage auxiliary metabolic genes and the redirection of cyanobacterial host carbon metabolism. Proc. Natl Acad. Sci. USA 108, E757–E764 (2011).

    Article  PubMed  Google Scholar 

  77. 77.

    Ledermann, B., Béjà, O. & Frankenberg‐Dinkel, N. New biosynthetic pathway for pink pigments from uncultured oceanic viruses. Environ. Microbiol. 18, 4337–4347 (2016).

    Article  CAS  PubMed  Google Scholar 

  78. 78.

    Rosenwasser, S., Ziv, C., Van Creveld, S. G. & Vardi, A. Virocell metabolism: metabolic innovations during host–virus interactions in the ocean. Trends Microbiol. 24, 821–832 (2016).

    Article  CAS  PubMed  Google Scholar 

  79. 79.

    Forterre, P. The virocell concept and environmental microbiology. ISME J. 7, 233–236 (2013).

    Article  CAS  PubMed  Google Scholar 

  80. 80.

    Puxty, R. J., Millard, A. D., Evans, D. J. & Scanlan, D. J. Viruses inhibit CO2 fixation in the most abundant phototrophs on Earth. Curr. Biol. 26, 1585–1589 (2016).

    Article  CAS  PubMed  Google Scholar 

  81. 81.

    Wikner, J., Vallino, J. J., Steward, G. F., Smith, D. C. & Azam, F. Nucleic acids from the host bacterium as a major source of nucleotides for three marine bacteriophages. FEMS Microbiol. Ecol. 12, 237–248 (1993).

    Article  CAS  Google Scholar 

  82. 82.

    Stazic, D., Pekarski, I., Kopf, M., Lindell, D. & Steglich, C. A novel strategy for exploitation of host RNase E activity by a marine cyanophage. Genetics 203, 1149–1159 (2016).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  83. 83.

    Ankrah, N. Y. D. et al. Phage infection of an environmentally relevant marine bacterium alters host metabolism and lysate composition. ISME J. 8, 1089–1100 (2014).

    Article  CAS  PubMed  Google Scholar 

  84. 84.

    Middelboe, M. & Jørgensen, N. O. Viral lysis of bacteria: an important source of dissolved amino acids and cell wall compounds. JMBA 86, 605–612 (2006).

    CAS  Google Scholar 

  85. 85.

    Middelboe, M. Bacterial growth rate and marine virus–host dynamics. Microb. Ecol. 40, 114–124 (2000).

    CAS  PubMed  Google Scholar 

  86. 86.

    Middelboe, M., Riemann, L., Steward, G. F., Hansen, V. & Nybroe, O. Virus-induced transfer of organic carbon between marine bacteria in a model community. Aquat. Microb. Ecol. 33, 1–10 (2003).

    Article  Google Scholar 

  87. 87.

    Shelford, E. J., Middelboe, M., Møller, E. F. & Suttle, C. A. Virus-driven nitrogen cycling enhances phytoplankton growth. Aquat. Microb. Ecol. 66, 41–46 (2012).

    Article  Google Scholar 

  88. 88.

    Poorvin, L., Rinta-Kanto, J., Hutchins, D. & Wilhelm, S. Viral release of iron and its bioavailability to marine plankton. Limnol. Oceanogr. 49, 1734–1741 (2004).

    Article  CAS  Google Scholar 

  89. 89.

    Breitbart, M. et al. Genomic analysis of uncultured marine viral communities. Proc. Natl Acad. Sci. USA 99, 14250–14255 (2002).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  90. 90.

    Mizuno, C. M., Rodriguez-Valera, F., Kimes, N. E. & Ghai, R. Expanding the marine virosphere using metagenomics. PLoS Genet. 9, e1003987 (2013).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  91. 91.

    Coutinho, F. et al. Marine viruses discovered via metagenomics shed light on viral strategies throughout the oceans. Nat. Commun. 8, 15955 (2017).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  92. 92.

    Roux, S. et al. Towards quantitative viromics for both double-stranded and single-stranded DNA viruses. PeerJ 4, e2777 (2016).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  93. 93.

    Paez-Espino, D. et al. Uncovering Earth’s virome. Nature 536, 425 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  94. 94.

    Kauffman, K. M. et al. A major lineage of non-tailed dsDNA viruses as unrecognized killers of marine bacteria. Nature 554, 118 (2018).

    Article  CAS  PubMed  Google Scholar 

  95. 95.

    Brum, J. R. et al. Patterns and ecological drivers of ocean viral communities. Science 348, 1261498 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  96. 96.

    Kristensen, D. M., Mushegian, A. R., Dolja, V. V. & Koonin, E. V. New dimensions of the virus world discovered through metagenomics. Trends Microbiol. 18, 11–19 (2010).

    Article  CAS  PubMed  Google Scholar 

  97. 97.

    Ignacio-Espinoza, J. C., Solonenko, S. A. & Sullivan, M. B. The global virome: not as big as we thought? Curr. Opin. Virol. 3, 566–571 (2013).

    Article  PubMed  Google Scholar 

  98. 98.

    Breitbart, M. & Rohwer, F. Here a virus, there a virus, everywhere the same virus? Trends Microbiol. 13, 278–284 (2005).

    Article  CAS  PubMed  Google Scholar 

  99. 99.

    Goldsmith, D., Brum, J., Hopkins, M., Carlson, C. & Breitbart, M. Water column stratification structures viral community diversity in the Sargasso Sea. Aquat. Microb. Ecol. 76, 85–94 (2015).

    Article  Google Scholar 

  100. 100.

    Zhan, Y., Huang, S., Voget, S., Simon, M. & Chen, F. A novel roseobacter phage possesses features of podoviruses, siphoviruses, prophages and gene transfer agents. Sci. Rep. 6, 30372 (2016).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  101. 101.

    Marston, M. F. & Martiny, J. B. Genomic diversification of marine cyanophages into stable ecotypes. Environ. Microbiol. 18, 4240–4253 (2016).

    Article  CAS  PubMed  Google Scholar 

  102. 102.

    Deng, L. et al. Viral tagging reveals discrete populations in Synechococcus viral genome sequence space. Nature 513, 242–245 (2014).

    Article  CAS  PubMed  Google Scholar 

  103. 103.

    Gregory, A. C. et al. Genomic differentiation among wild cyanophages despite widespread horizontal gene transfer. BMC Genomics 17, 930 (2016).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  104. 104.

    Angly, F. et al. Genomic analysis of multiple Roseophage SIO1 strains. Environ. Microbiol. 11, 2863–2873 (2009).

    Article  CAS  PubMed  Google Scholar 

  105. 105.

    Kalatzis, P. G. et al. Stumbling across the same phage: comparative genomics of widespread temperate phages infecting the fish pathogen Vibrio anguillarum. Viruses 9, 122 (2017).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  106. 106.

    Pagarete, A. et al. Strong seasonality and interannual recurrence in marine myovirus communities. Appl. Environ. Microbiol. 79, 6253–6259 (2013).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  107. 107.

    Chow, C. E. T. & Fuhrman, J. A. Seasonality and monthly dynamics of marine myovirus communities. Environ. Microbiol. 14, 2171–2183 (2012).

    PubMed  PubMed Central  Article  Google Scholar 

  108. 108.

    Chow, C.-E. T., Kim, D. Y., Sachdeva, R., Caron, D. A. & Fuhrman, J. A. Top-down controls on bacterial community structure: microbial network analysis of bacteria, T4-like viruses and protists. ISME J. 8, 816–829 (2014).

    Article  CAS  PubMed  Google Scholar 

  109. 109.

    Goldsmith, D., Parsons, R., Beyene, D., Salamon, P. & Breitbart, M. Deep sequencing of the viral phoH gene reveals seasonal variations, depth-specific composition, and persistent dominance of the same viral phoH genes in the Sargasso Sea. PeerJ 3, e997 (2015).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  110. 110.

    Martiny, J. B., Riemann, L., Marston, M. F. & Middelboe, M. Antagonistic coevolution of marine planktonic viruses and their hosts. Annu. Rev. Mar. Sci. 6, 393–414 (2014).

    Article  Google Scholar 

  111. 111.

    Koskella, B. & Brockhurst, M. A. Bacteria–phage coevolution as a driver of ecological and evolutionary processes in microbial communities. FEMS Microbiol. Rev. 38, 916–931 (2014).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  112. 112.

    Thingstad, T. F., Pree, B., Giske, J. & Våge, S. What difference does it make if viruses are strain-, rather than species-specific? Front. Microbiol. 6, 320 (2015).

    PubMed  PubMed Central  Article  Google Scholar 

  113. 113.

    Thingstad, T. F., Våge, S., Storesund, J. E., Sandaa, R.-A. & Giske, J. A theoretical analysis of how strain-specific viruses can control microbial species diversity. Proc. Natl Acad. Sci. USA 111, 7813–7818 (2014).

    Article  CAS  PubMed  Google Scholar 

  114. 114.

    Comeau, A. M., Bertrand, C., Letarov, A., Tétart, F. & Krisch, H. Modular architecture of the T4 phage superfamily: a conserved core genome and a plastic periphery. Virology 362, 384–396 (2007).

    Article  CAS  PubMed  Google Scholar 

  115. 115.

    Sullivan, M. B. et al. Genomic analysis of oceanic cyanobacterial myoviruses compared with T4-like myoviruses from diverse hosts and environments. Environ. Microbiol. 12, 3035–3056 (2010).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  116. 116.

    Rodriguez-Valera, F., Martin-Cuadrado, A. B., Beltran Rodriguez-Brito, L. P., Thingstad, T. F. & Forest Rohwer, A. M. Explaining microbial population genomics through phage predation. Nat. Rev. Microbiol. 7, 828–836 (2009).

    Article  CAS  PubMed  Google Scholar 

  117. 117.

    Middelboe, M., Holmfeldt, K., Riemann, L., Nybroe, O. & Haaber, J. Bacteriophages drive strain diversification in a marine Flavobacterium: implications for phage resistance and physiological properties. Environ. Microbiol. 11, 1971–1982 (2009).

    Article  CAS  PubMed  Google Scholar 

  118. 118.

    Needham, D. M., Sachdeva, R. & Fuhrman, J. A. Ecological dynamics and co-occurrence among marine phytoplankton, bacteria and myoviruses shows microdiversity matters. ISME J. 11, 1614–1629 (2017).

    PubMed  PubMed Central  Article  Google Scholar 

  119. 119.

    Brown, M. V. & Fuhrman, J. A. Marine bacterial microdiversity as revealed by internal transcribed spacer analysis. Aquat. Microb. Ecol. 41, 15–23 (2005).

    Article  Google Scholar 

  120. 120.

    Fuhrman, J. A., Cram, J. A. & Needham, D. M. Marine microbial community dynamics and their ecological interpretation. Nat. Rev. Microbiol. 13, 133 (2015).

    Article  CAS  PubMed  Google Scholar 

  121. 121.

    Marston, M. F. & Amrich, C. G. Recombination and microdiversity in coastal marine cyanophages. Environ. Microbiol. 11, 2893–2903 (2009).

    Article  PubMed  Google Scholar 

  122. 122.

    Needham, D. M. et al. Short-term observations of marine bacterial and viral communities: patterns, connections and resilience. ISME J. 7, 1274–1285 (2013).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  123. 123.

    Zhao, Y. et al. Abundant SAR11 viruses in the ocean. Nature 494, 357–360 (2013).

    Article  CAS  PubMed  Google Scholar 

  124. 124.

    Kang, I., Oh, H.-M., Kang, D. & Cho, J.-C. Genome of a SAR116 bacteriophage shows the prevalence of this phage type in the oceans. Proc. Natl Acad Sci. USA 110, 12343–12348 (2013).

    Article  PubMed  Google Scholar 

  125. 125.

    Breitbart, M. Marine viruses: truth or dare. Annu. Rev. Mar. Sci. 4, 425–448 (2012).

    Article  Google Scholar 

  126. 126.

    Vik, D. R. et al. Putative archaeal viruses from the mesopelagic ocean. PeerJ 5, e3428 (2017).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  127. 127.

    Ahlgren, N. A. et al. Genome and epigenome of a novel marine Thaumarchaeota strain suggest viral infection, phosphorothioation DNA modification and multiple restriction systems. Environ. Microbiol. 19, 2434–2452 (2017).

    Article  CAS  PubMed  Google Scholar 

  128. 128.

    Labonté, J. M. et al. Single-cell genomics-based analysis of virus–host interactions in marine surface bacterioplankton. ISME J. 9, 2386–2399 (2015).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  129. 129.

    Martínez-García, M., Santos, F., Moreno-Paz, M., Parro, V. & Antón, J. Unveiling viral–host interactions within the ‘microbial dark matter’. Nat. Commun. 5, 4542 (2014).

    Article  CAS  PubMed  Google Scholar 

  130. 130.

    Nigro, O. D. et al. Viruses in the oceanic basement. mBio 8, e02129–16 (2017).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  131. 131.

    Engelhardt, T., Orsi, W. D. & Jørgensen, B. B. Viral activities and life cycles in deep subseafloor sediments. Environ. Microbiol. Rep. 7, 868–873 (2015).

    Article  CAS  PubMed  Google Scholar 

  132. 132.

    Ren, J., Ahlgren, N., Lu, Y., Fuhrman, J. & Sun, F. VirFinder: a novel k-mer based tool for identifying viral sequences from assembled metagenomic data. Microbiome 5, 69 (2017).

    PubMed  PubMed Central  Article  Google Scholar 

  133. 133.

    Rodriguez-Valera, F., Mizuno, C. M. & Ghai, R. Tales from a thousand and one phages. Bacteriophage 4, e1003987 (2014).

    Article  Google Scholar 

  134. 134.

    Brum, J. R. & Sullivan, M. B. Rising to the challenge: accelerated pace of discovery transforms marine virology. Nat. Rev. Microbiol. 13, 147–159 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  135. 135.

    Nishimura, Y. et al. Environmental viral genomes shed new light on virus-host interactions in the ocean. mSphere 2, e00359-16 (2017).

    PubMed  PubMed Central  Article  Google Scholar 

  136. 136.

    Mizuno, C. M., Ghai, R., Saghaï, A., López-García, P. & Rodriguez-Valera, F. Genomes of abundant and widespread viruses from the deep ocean. mBio 7, e00805–16 (2016).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  137. 137.

    Roux, S. et al. Ecology and evolution of viruses infecting uncultivated SUP05 bacteria as revealed by single-cell-and meta-genomics. eLife 3, e03125 (2014).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  138. 138.

    Chow, C.-E. T., Winget, D. M., White, R. A. III, Hallam, S. J. & Suttle, C. A. Combining genomic sequencing methods to explore viral diversity and reveal potential virus-host interactions. Front. Microbiol. 6, 265 (2015).

    PubMed  PubMed Central  Google Scholar 

  139. 139.

    Martinez-Hernandez, F. et al. Single-virus genomics reveals hidden cosmopolitan and abundant viruses. Nat. Commun. 8, 15892 (2017).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  140. 140.

    Anderson, R. E., Brazelton, W. J. & Baross, J. A. Using CRISPRs as a metagenomic tool to identify microbial hosts of a diffuse flow hydrothermal vent viral assemblage. FEMS Microbiol. Ecol. 77, 120–133 (2011).

    Article  CAS  PubMed  Google Scholar 

  141. 141.

    Allers, E. et al. Single-cell and population level viral infection dynamics revealed by phageFISH, a method to visualize intracellular and free viruses. Environ. Microbiol. 15, 2306–2318 (2013).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  142. 142.

    Baran, N., Goldin, S., Maidanik, I. & Lindell, D. Quantification of diverse virus populations in the environment using the polony method. Nat. Microbiol. 3, 62–72 (2018).

    Article  CAS  PubMed  Google Scholar 

  143. 143.

    Tadmor, A. D., Ottesen, E. A., Leadbetter, J. R. & Phillips, R. Probing individual environmental bacteria for viruses by using microfluidic digital PCR. Science 333, 58–62 (2011).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  144. 144.

    Edwards, R. A., McNair, K., Faust, K., Raes, J. & Dutilh, B. E. Computational approaches to predict bacteriophage–host relationships. FEMS Microbiol. Rev. 40, 258–272 (2015).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  145. 145.

    Roux, S., Enault, F., Hurwitz, B. L. & Sullivan, M. B. VirSorter: mining viral signal from microbial genomic data. PeerJ 3, e985 (2015).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  146. 146.

    Galiez, C., Siebert, M., Enault, F., Vincent, J. & Söding, J. WIsH: who is the host? Predicting prokaryotic hosts from metagenomic phage contigs. Bioinformatics 33, 3113–3114 (2017).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  147. 147.

    Zhang, M. et al. Prediction of virus-host infectious association by supervised learning methods. BMC Bioinformatics 18, 60 (2017).

    PubMed  PubMed Central  Article  Google Scholar 

  148. 148.

    Ahlgren, N. A., Ren, J., Lu, Y. Y., Fuhrman, J. A. & Sun, F. Alignment-free oligonucleotide frequency dissimilarity measure improves prediction of hosts from metagenomically-derived viral sequences. Nucleic Acids Res. 45, 39–53 (2016).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  149. 149.

    Flores, C. O., Meyer, J. R., Valverde, S., Farr, L. & Weitz, J. S. Statistical structure of host–phage interactions. Proc. Natl Acad. Sci. USA 108, E288–E297 (2011).

    Article  PubMed  Google Scholar 

  150. 150.

    Flores, C. O., Valverde, S. & Weitz, J. S. Multi-scale structure and geographic drivers of cross-infection within marine bacteria and phages. ISME J. 7, 520–532 (2013).

    Article  PubMed  Google Scholar 

  151. 151.

    Weitz, J. S. et al. Phage–bacteria infection networks. Trends Microbiol. 21, 82–91 (2013).

    Article  CAS  PubMed  Google Scholar 

  152. 152.

    Diaz-Munoz, S. L. Viral coinfection is shaped by host ecology and virus–virus interactions across diverse microbial taxa and environments. Virus Evol. 3, vex011 (2017).

    PubMed  PubMed Central  Article  Google Scholar 

  153. 153.

    Lima-Mendez, G. et al. Determinants of community structure in the global plankton interactome. Science 348, 1262073 (2015).

    Article  CAS  PubMed  Google Scholar 

  154. 154.

    Stoddard, L., Martiny, J. & Marston, M. Selection and characterization of cyanophage resistance in marine Synechococcus strains. Appl. Environ. Microbiol. 73, 5516–5522 (2007).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  155. 155.

    Jover, L. F., Cortez, M. H. & Weitz, J. S. Mechanisms of multi-strain coexistence in host–phage systems with nested infection networks. J. Theor. Biol. 332, 65–77 (2013).

    Article  PubMed  Google Scholar 

  156. 156.

    Korytowski, D. A. & Smith, H. L. How nested and monogamous infection networks in host-phage communities come to be. Theor. Ecol. 8, 111–120 (2015).

    Article  Google Scholar 

  157. 157.

    Avrani, S., Wurtzel, O., Sharon, I., Sorek, R. & Lindell, D. Genomic island variability facilitates Prochlorococcus-virus coexistence. Nature 474, 604–608 (2011).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  158. 158.

    Marston, M. F. et al. Rapid diversification of coevolving marine Synechococcus and a virus. Proc. Natl Acad. Sci. USA 109, 4544–4549 (2012).

    PubMed  PubMed Central  Article  Google Scholar 

  159. 159.

    Tzipilevich, E., Habusha, M. & Ben-Yehuda, S. Acquisition of phage sensitivity by bacteria through exchange of phage receptors. Cell 168, 186–199 (2017).

    Article  CAS  PubMed  Google Scholar 

  160. 160.

    Holmfeldt, K., Howard-Varona, C., Solonenko, N. & Sullivan, M. B. Contrasting genomic patterns and infection strategies of two co-existing Bacteroidetes podovirus genera. Environ. Microbiol. 16, 2501–2513 (2014).

    Article  CAS  PubMed  Google Scholar 

  161. 161.

    Holmfeldt, K., Middelboe, M., Nybroe, O. & Riemann, L. Large variabilities in host strain susceptibility and phage host range govern interactions between lytic marine phages and their Flavobacterium hosts. Appl. Environ. Microbiol. 73, 6730–6739 (2007).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  162. 162.

    Holmfeldt, K. et al. Large-scale maps of variable infection efficiencies in aquatic Bacteroidetes phage-host model systems. Environ. Microbiol. 18, 3949–3961 (2016).

    Article  CAS  PubMed  Google Scholar 

  163. 163.

    Doron, S. et al. Transcriptome dynamics of a broad host-range cyanophage and its hosts. ISME J. 10, 1437–1455 (2016).

    Article  CAS  PubMed  Google Scholar 

  164. 164.

    Howard-Varona, C. et al. Regulation of infection efficiency in a globally abundant marine Bacteriodetes virus. ISME J. 11, 284–295 (2017).

    Article  CAS  PubMed  Google Scholar 

  165. 165.

    Short, C. M., Rusanova, O. & Short, S. M. Quantification of virus genes provides evidence for seed-bank populations of phycodnaviruses in Lake Ontario, Canada. ISME J. 5, 810–821 (2011).

    Article  CAS  PubMed  Google Scholar 

  166. 166.

    Sullivan, M., Coleman, M., Weigele, P., Rohwer, F. & Chisholm, S. Three Prochlorococcus cyanophage genomes: signature features and ecological interpretations. PLoS Biol. 3, 790–806 (2005).

    Article  CAS  Google Scholar 

  167. 167.

    Marine, R. L., Nasko, D. J., Wray, J., Polson, S. W. & Wommack, K. E. Novel chaperonins are prevalent in the virioplankton and demonstrate links to viral biology and ecology. ISME J. 11, 2479 (2017).

    PubMed  PubMed Central  Article  Google Scholar 

  168. 168.

    Thingstad, T. F. & Lignell, R. Theoretical models for the control of bacterial growth rate, abundance, diversity and carbon demand. Aquat. Microb. Ecol. 13, 19–27 (1997).

    Article  Google Scholar 

  169. 169.

    Winter, C., Bouvier, T., Weinbauer, M. & Thingstad, T. Trade-offs between competition and defense specialists among unicellular plankton organisms: the “killing the winner” hypothesis revisited. Microb. Molec. Biol. Rev. 74, 42–57 (2010).

    Article  CAS  Google Scholar 

  170. 170.

    Thingstad, T. Elements of a theory for the mechanisms controlling abundance, diversity, and biogeochemical role of lytic bacterial viruses in aquatic systems. Limnol. Oceanogr. 45, 1320–1328 (2000).

    Article  Google Scholar 

  171. 171.

    Comeau, A. M. & Krisch, H. M. War is peace—dispatches from the bacterial and phage killing fields. Curr. Opin. Microbiol. 8, 488–494 (2005).

    Article  CAS  PubMed  Google Scholar 

  172. 172.

    Stern, A. & Sorek, R. The phage‐host arms race: shaping the evolution of microbes. Bioessays 33, 43–51 (2011).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  173. 173.

    Rodriguez-Brito, B. et al. Viral and microbial community dynamics in four aquatic environments. ISME J. 4, 739–751 (2010).

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

The authors thank D. Goldsmith, P. Salamon and C. Silveira for helpful discussions regarding the royal family model, and K. M. Scott for input regarding Fig. 5. M.B. was funded by grants DEB-1555854, IOS-1456301 and OCE-1722761 from the National Science Foundation. K.M. was supported by a National Science Foundation Graduate Research Fellowship (Award No. 3900101301). C.B. was supported by the Linton Tibbetts Endowed Graduate Student Fellowship. N.A.S. was supported by the Gulf Oceanographic Charitable Trust Endowed Fellowship.

Author information

Affiliations

Authors

Contributions

All authors contributed to the writing, editing and preparation of figures for this manuscript.

Corresponding author

Correspondence to Mya Breitbart.

Ethics declarations

Competing interests

The authors declare no competing interests.

Additional information

Publisher's note: Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Breitbart, M., Bonnain, C., Malki, K. et al. Phage puppet masters of the marine microbial realm. Nat Microbiol 3, 754–766 (2018). https://doi.org/10.1038/s41564-018-0166-y

Download citation

Further reading

Search

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing