Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Review Article
  • Published:

Metabolic and biogeochemical consequences of viral infection in aquatic ecosystems

Nature Reviews Microbiology volume 18, pages 21–34 (2020)Cite this article

Subjects

Abstract

Ecosystems are controlled by ‘bottom-up’ (resources) and ‘top-down’ (predation) forces. Viral infection is now recognized as a ubiquitous top-down control of microbial growth across ecosystems but, at the same time, cell death by viral predation influences, and is influenced by, resource availability. In this Review, we discuss recent advances in understanding the biogeochemical impact of viruses, focusing on how metabolic reprogramming of host cells during lytic viral infection alters the flow of energy and nutrients in aquatic ecosystems. Our synthesis revealed several emerging themes. First, viral infection transforms host metabolism, in part through virus-encoded metabolic genes; the functions performed by these genes appear to alleviate energetic and biosynthetic bottlenecks to viral production. Second, viral infection depends on the physiological state of the host cell and on environmental conditions, which are challenging to replicate in the laboratory. Last, metabolic reprogramming of infected cells and viral lysis alter nutrient cycling and carbon export in the oceans, although the net impacts remain uncertain. This Review highlights the need for understanding viral infection dynamics in realistic physiological and environmental contexts to better predict their biogeochemical consequences.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Fig. 1: Remodelling of host metabolic pathways during viral infection.
Fig. 2: Relationships between viral productivity and host physiology or environment.
Fig. 3: The role of viruses in marine carbon and nutrient cycling.

Similar content being viewed by others

References

  1. Jacob, F. The Logic of Life: A History of Heredity (Princeton Univ. Press, 1973).

  2. Falkowski, P. G., Fenchel, T. & DeLong, E. F. The microbial engines that drive Earth’s biogeochemical cycles. Science 320, 1034–1039 (2008).

    CAS  PubMed  Google Scholar 

  3. Pomeroy, L. R. The ocean’s food web, a changing paradigm. Bioscience 24, 499–504 (1974).

    Google Scholar 

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

    CAS  PubMed  Google Scholar 

  5. Wilhelm, S. W. & Suttle, C. A. Viruses and nutrient cycles in the sea. Bioscience 49, 781–788 (1999).

    Google Scholar 

  6. Bidle, K. D. Programmed cell death in unicellular phytoplankton. Curr. Biol. 26, R594–R607 (2016).

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  11. Angly, F. E. et al. The marine viromes of four oceanic regions. PLOS Biol. 4, 2121–2131 (2006).

    CAS  Google Scholar 

  12. Krupovic, M., Cvirkaite-Krupovic, V., Iranzo, J., Prangishvili, D. & Koonin, E. V. Viruses of archaea: structural, functional, environmental and evolutionary genomics. Virus Res. 244, 181–193 (2018).

    CAS  PubMed  Google Scholar 

  13. Paez-Espino, D. et al. Uncovering Earth’s virome. Nature 536, 425–430 (2016).

    CAS  PubMed  Google Scholar 

  14. Gregory, A. C. et al. Marine DNA viral macro- and microdiversity from pole to pole. Cell 177, 1109–1123 (2019).

    CAS  PubMed  Google Scholar 

  15. Kim, J.-G. et al. Spindle-shaped viruses infect marine ammonia-oxidizing thaumarchaea. Proc. Natl Acad. Sci. USA 116, 15645–15650 (2019). This study presents the first reported isolation of viruses infecting widespread marine archaea, demonstrating the continuation of ammonium oxidation activity during infection and a chronic infection strategy distinct from that of the lytic bacteriophage.

    CAS  PubMed  Google Scholar 

  16. Derelle, E. et al. Diversity of viruses infecting the green microalga Ostreococcus lucimarinus. J. Virol. 89, 5812–5821 (2015).

    CAS  PubMed  PubMed Central  Google Scholar 

  17. Moniruzzaman, M. et al. Genome of brown tide virus (AaV), the little giant of the Megaviridae, elucidates NCLDV genome expansion and host–virus coevolution. Virology 466–467, 60–70 (2014).

    PubMed  Google Scholar 

  18. Santini, S. et al. Genome of Phaeocystis globosa virus PgV-16T highlights the common ancestry of the largest known DNA viruses infecting eukaryotes. Proc. Natl Acad. Sci. USA 110, 10800–10805 (2013).

    CAS  PubMed  Google Scholar 

  19. Deeg, C. M., Chow, C. E. T. & Suttle, C. A. The kinetoplastid-infecting Bodo saltans virus (Bsv), a window into the most abundant giant viruses in the sea. eLife 7, e33014 (2018).

    PubMed  PubMed Central  Google Scholar 

  20. Claverie, J.-M. & Abergel, C. Mimiviridae: an expanding family of highly diverse large dsDNA viruses infecting a wide phylogenetic range of aquatic eukaryotes. Viruses 10, 506 (2018).

    PubMed Central  Google Scholar 

  21. Coy, S., Gann, E., Pound, H., Short, S. & Wilhelm, S. Viruses of eukaryotic algae: diversity, methods for detection, and future directions. Viruses 10, 487 (2018).

    PubMed Central  Google Scholar 

  22. Hingamp, P. et al. Exploring nucleo-cytoplasmic large DNA viruses in Tara Oceans microbial metagenomes. ISME J. 7, 1678–1695 (2013).

    CAS  PubMed  PubMed Central  Google Scholar 

  23. Needham, D. M. et al. A distinct lineage of giant viruses brings a rhodopsin photosystem to unicellular marine predators. Proc. Natl Acad. Sci. USA 116, 20574–20583 (2019).

  24. Lindell, D. et al. Genome-wide expression dynamics of a marine virus and host reveal features of co-evolution. Nature 449, 83–86 (2007).

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  26. Morimoto, D., Kimura, S., Sako, Y. & Yoshida, T. Transcriptome analysis of a bloom-forming cyanobacterium Microcystis aeruginosa during Ma-LMM01 phage infection. Front. Microbiol. 9, 2 (2018).

    PubMed  PubMed Central  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  28. Howard-Varona, C. et al. Multiple mechanisms drive phage infection efficiency in nearly identical hosts. ISME J. 12, 1605–1618 (2018).

    PubMed  PubMed Central  Google Scholar 

  29. Allen, M. J. et al. Locus-specific gene expression pattern suggests a unique propagation strategy for a giant algal virus. J. Virol. 80, 7699–7705 (2006).

    CAS  PubMed  PubMed Central  Google Scholar 

  30. Rosenwasser, S. et al. Rewiring host lipid metabolism by large viruses determines the fate of Emiliania huxleyi, a bloom-forming alga in the ocean. Plant Cell 26, 2689–2707 (2014).

    CAS  PubMed  PubMed Central  Google Scholar 

  31. Bachy, C. et al. Transcriptional responses of the marine green alga Micromonas pusilla and an infecting prasinovirus under different phosphate conditions. Environ. Microbiol. 20, 2898–2912 (2018).

    CAS  PubMed  Google Scholar 

  32. Moniruzzaman, M., Gann, E. R. & Wilhelm, S. W. Infection by a giant virus (AaV) induces widespread physiological reprogramming in Aureococcus anophagefferens CCMP1984-A harmful bloom algae. Front. Microbiol. 9, 752 (2018).

    PubMed  PubMed Central  Google Scholar 

  33. 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).

    CAS  PubMed  Google Scholar 

  34. Rosenwasser, S. et al. Unmasking cellular response of a bloom-forming alga to viral infection by resolving expression profiles at a single-cell level. PLOS Pathog. 15, e1007708 (2019).

    CAS  PubMed  PubMed Central  Google Scholar 

  35. Sieradzki, E. T., Ignacio-Espinoza, J. C., Needham, D. M., Fichot, E. B. & Fuhrman, J. A. Dynamic marine viral infections and major contribution to photosynthetic processes shown by regional and seasonal picoplankton metatranscriptomes. Nat. Commun. 10, 1169 (2019).

    PubMed  PubMed Central  Google Scholar 

  36. Moniruzzaman, M. et al. Virus–host relationships of marine single-celled eukaryotes resolved from metatranscriptomics. Nat. Commun. 8, 16054 (2017).

    CAS  PubMed  PubMed Central  Google Scholar 

  37. Aylward, F. O. et al. Diel cycling and long-term persistence of viruses in the ocean’s euphotic zone. Proc. Natl Acad. Sci. USA 114, 11446–11451 (2017).

    CAS  PubMed  Google Scholar 

  38. Kolody, B. C. et al. Diel transcriptional response of a California Current plankton microbiome to light, low iron, and enduring viral infection. ISME J. 13, 2817–2833 (2019).

  39. Kutter, E. et al. From host to phage metabolism: hot tales of phage T4’s takeover of E. coli. Viruses 10, 387 (2018).

    PubMed Central  Google Scholar 

  40. Yin, J. & Redovich, J. Kinetic modeling of virus growth in cells. Microbiol. Mol. Biol. Rev. 82, e00066-17 (2018).

    PubMed  PubMed Central  Google Scholar 

  41. Thamatrakoln, K. et al. Light regulation of coccolithophore host–virus interactions. New Phytol. 221, 1289–1302 (2019). Based on photophysiology and biochemical measurements during E. huxleyi viral infection, this study suggests that viral replication is controlled by a light-dependent trade-off between host nucleotide recycling and de novo synthesis.

    CAS  PubMed  Google Scholar 

  42. Ziv, C. et al. Viral serine palmitoyltransferase induces metabolic switch in sphingolipid biosynthesis and is required for infection of a marine alga. Proc. Natl Acad. Sci. USA 113, E1907–E1916 (2016).

    CAS  PubMed  Google Scholar 

  43. Malitsky, S. et al. Viral infection of the marine alga Emiliania huxleyi triggers lipidome remodeling and induces the production of highly saturated triacylglycerol. New Phytol. 210, 88–96 (2016).

    CAS  PubMed  Google Scholar 

  44. Vardi, A. et al. Host–virus dynamics and subcellular controls of cell fate in a natural coccolithophore population. Proc. Natl Acad. Sci. USA 109, 19327–19332 (2012).

    CAS  PubMed  Google Scholar 

  45. Nissimov, J. I. et al. Dynamics of transparent exopolymer particle (TEP) production and aggregation during viral infection of the coccolithophore, Emiliania huxleyi. Environ. Microbiol. 20, 2880–2897 (2018).

    CAS  PubMed  Google Scholar 

  46. 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). This paper shows that cyanophages encode a Calvin cycle inhibitor and transaldolase with enzymological properties different from their host homologues, demonstrating the importance of the pentose phosphate pathway during infection.

    CAS  PubMed  Google Scholar 

  47. 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). This paper uses metabolomics to quantify redirection of metabolic fluxes during phage infection of a marine α-proteobacterium, and consequent compositional alteration of dissolved material released by lysis.

    CAS  PubMed  Google Scholar 

  48. Schleyer, G. et al. In plaque-mass spectrometry imaging of a bloom-forming alga during viral infection reveals a metabolic shift towards odd-chain fatty acid lipids. Nat. Microbiol. 4, 527–538 (2019).

    CAS  PubMed  PubMed Central  Google Scholar 

  49. Hunter, J. E., Frada, M. J., Fredricks, H. F., Vardi, A. & Van Mooy, B. A. S. Targeted and untargeted lipidomics of Emiliania huxleyi viral infection and life cycle phases highlights molecular biomarkers of infection, susceptibility, and ploidy. Front. Mar. Sci. 2, 81 (2015).

    Google Scholar 

  50. Schieler, B. M. et al. Nitric oxide production and antioxidant function during viral infection of the coccolithophore Emiliania huxleyi. ISME J. 13, 1019–1031 (2019).

    CAS  PubMed  PubMed Central  Google Scholar 

  51. Fedida, A. & Lindell, D. Two Synechococcus genes, two different effects on cyanophage infection. Viruses 9, 136 (2017).

    PubMed Central  Google Scholar 

  52. Waldbauer, J. R. et al. Nitrogen sourcing during viral infection of marine cyanobacteria. Proc. Natl Acad. Sci. USA 116, 15590–15595 (2019). This proteomics study quantitatively tracks nitrogen incorporation during phage infection of Synechococcus, showing that substantial amounts of phage protein nitrogen are acquired from the environment after infection begins and incorporated via de novo amino acid synthesis.

    CAS  PubMed  Google Scholar 

  53. Doron, S. et al. Systematic discovery of antiphage defense systems in the microbial pangenome. Science 359, eaar4120 (2018).

    PubMed  PubMed Central  Google Scholar 

  54. Koonin, E. V., Makarova, K. S. & Wolf, Y. I. Evolutionary genomics of defense systems in Archaea and Bacteria. Annu. Rev. Microbiol. 71, 233–261 (2017).

    CAS  PubMed  PubMed Central  Google Scholar 

  55. Schatz, D. et al. Hijacking of an autophagy-like process is critical for the life cycle of a DNA virus infecting oceanic algal blooms. New Phytol. 204, 854–863 (2014).

    CAS  PubMed  PubMed Central  Google Scholar 

  56. Hoehler, T. M. & Jørgensen, B. B. Microbial life under extreme energy limitation. Nat. Rev. Microbiol. 11, 83–94 (2013).

    CAS  PubMed  Google Scholar 

  57. Kirchman, D. L. Processes in Microbial Ecology 99–116 (Oxford Univ. Press, 2012).

  58. Cohen, S. S. Growth requirements of bacterial viruses. Bacteriol. Rev. 13, 1–24 (1949).

    CAS  PubMed  PubMed Central  Google Scholar 

  59. Hadas, H., Einav, M., Fishov, I. & Zaritsky, A. Bacteriophage T4 development depends on the physiology of its host Escherichia coli. Microbiology 143, 179–185 (1997).

    CAS  PubMed  Google Scholar 

  60. You, L., Suthers, P. F. & Yin, J. Effects of Escherichia coli physiology on growth of phage T7 in vivo and in silico. J. Bacteriol. 184, 1888–1894 (2002).

    CAS  PubMed  PubMed Central  Google Scholar 

  61. Van Etten, J. L., Burbank, D. E., Xia, Y. & Meints, R. H. Growth cycle of a virus, PBCV-1, that infects Chlorella-like algae. Virology 126, 117–125 (1983).

    PubMed  Google Scholar 

  62. Piedade, G. J., Wesdorp, E. M., Montenegro-Borbolla, E., Maat, D. S. & Brussaard, C. P. D. Influence of irradiance and temperature on the virus MpoV-45T infecting the arctic picophytoplankter Micromonas polaris. Viruses 10, 676 (2018).

    CAS  PubMed Central  Google Scholar 

  63. Bratbak, G., Jacobsen, A., Heldal, M., Nagasaki, K. & Thingstad, T. F. Virus production in Phaeocystis pouchetii and its relation to host cell growth and nutrition. Aquat. Microb. Ecol. 16, 1–9 (1998).

    Google Scholar 

  64. Baudoux, A.-C. & Brussaard, C. P. D. Influence of irradiance on virus–algal host interactions. J. Phycol. 44, 902–908 (2008).

    PubMed  Google Scholar 

  65. Brown, C. M., Campbell, D. A. & Lawrence, J. E. Resource dynamics during infection of Micromonas pusilla by virus MpV-Sp1. Environ. Microbiol. 9, 2720–2727 (2007).

    CAS  PubMed  Google Scholar 

  66. Maat, D. S., de Blok, R. & Brussaard, C. P. D. Combined phosphorus limitation and light stress prevent viral proliferation in the phytoplankton species Phaeocystis globosa, but not in Micromonas pusilla. Front. Mar. Sci. 3, 160 (2016).

    Google Scholar 

  67. Maat, D. S. et al. Characterization and temperature dependence of arctic Micromonas polaris viruses. Viruses 9, 134 (2017).

    PubMed Central  Google Scholar 

  68. Demory, D. et al. Temperature is a key factor in Micromonas–virus interactions. ISME J. 11, 601–612 (2017).

    CAS  PubMed  PubMed Central  Google Scholar 

  69. Kendrick, B. J. et al. Temperature-induced viral resistance in Emiliania huxleyi (Prymnesiophyceae). PLOS ONE 9, e112134 (2014).

    PubMed  PubMed Central  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  71. Wilson, W. H., Carr, N. G. & Mann, N. H. The effect of phosphate status on the kinetics of cyanophage infection in the oceanic cyanobacterium Synechococcus sp. WH7803. J. Phycol. 32, 506–516 (1996).

    CAS  Google Scholar 

  72. Maat, D. S. & Brussaard, C. P. D. Both phosphorus and nitrogen limitation constrain viral proliferation in marine phytoplankton. Aquat. Microb. Ecol. 77, 87–97 (2016).

    Google Scholar 

  73. Slagter, H. A., Gerringa, L. J. A. & Brussaard, C. P. D. Phytoplankton virus production negatively affected by iron limitation. Front. Mar. Sci. 3, 156 (2016).

    Google Scholar 

  74. Kranzler, C. F. et al. Silicon limitation facilitates virus infection and mortality of marine diatoms. Nat. Microbiol. https://doi.org/10.1038/s41564-019-0502-x (2019). Using both cultured isolates and field observations, this study shows that silicon stress can accelerate virus-induced mortality of marine diatoms, potentially promoting nutrient recycling via the viral shunt.

    Article  PubMed  Google Scholar 

  75. Padan, E. & Shilo, M. Cyanophages–viruses attacking blue–green algae. Bacteriol. Rev. 37, 343–370 (1973).

    CAS  PubMed  PubMed Central  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  77. Thompson, L. R., Zeng, Q. & Chisholm, S. W. Gene expression patterns during light and dark infection of Prochlorococcus by cyanophage. PLOS ONE 11, e0165375 (2016).

    PubMed  PubMed Central  Google Scholar 

  78. Puxty, R. J., Evans, D. J., Millard, A. D. & Scanlan, D. J. Energy limitation of cyanophage development: implications for marine carbon cycling. ISME J. 12, 1273–1286 (2018). This study demonstrates that cyanophages modulate expression of photosynthesis-related accessory metabolic genes in response to light intensity, suggesting energy limitation of phage productivity and a basis for diel and seasonal patterns of virus-induced mortality.

    CAS  PubMed  PubMed Central  Google Scholar 

  79. Ginzburg, D., Padan, E. & Shilo, M. Effect of cyanophage infection on CO2 photoassimilation in Plectonema boryanum. J. Virol. 2, 695–701 (1968).

    CAS  PubMed  PubMed Central  Google Scholar 

  80. Adolph, K. W. & Haselkorn, R. Photosynthesis and the development of blue–green algal virus N-1. Virology 47, 370–374 (1972).

    CAS  PubMed  Google Scholar 

  81. Mackenzie, J. J. & Haselkorn, R. Photosynthesis and the development of blue–green algal virus SM-1. Virology 49, 517–521 (1972).

    CAS  PubMed  Google Scholar 

  82. 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).

    CAS  PubMed  Google Scholar 

  83. Mahmoudabadi, G., Milo, R. & Phillips, R. The energetic cost of building a virus. Proc. Natl Acad. Sci. USA 114, E4324–E4333 (2017).

    CAS  PubMed  Google Scholar 

  84. Sharon, I. et al. Photosystem I gene cassettes are present in marine virus genomes. Nature 461, 258–262 (2009).

    CAS  PubMed  PubMed Central  Google Scholar 

  85. Fridman, S. et al. A myovirus encoding both photosystem I and II proteins enhances cyclic electron flow in infected Prochlorococcus cells. Nat. Microbiol. 2, 1350–1357 (2017).

    CAS  PubMed  Google Scholar 

  86. Mann, N. H. Phages of the marine cyanobacterial picophytoplankton. FEMS Microbiol. Rev. 27, 17–34 (2003).

    CAS  PubMed  Google Scholar 

  87. Lindell, D. et al. Transfer of photosynthesis genes to and from Prochlorococcus viruses. Proc. Natl Acad. Sci. USA 101, 11013–11018 (2004).

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  91. Ledermann, B. et al. Evolution and molecular mechanism of four-electron reducing ferredoxin-dependent bilin reductases from oceanic phages. FEBS J. 285, 339–356 (2018).

    CAS  PubMed  Google Scholar 

  92. Clokie, M. R. J. et al. Transcription of a ‘photosynthetic’ T4-type phage during infection of a marine cyanobacterium. Environ. Microbiol. 8, 827–835 (2006).

    CAS  PubMed  Google Scholar 

  93. Hellweger, F. L. Carrying photosynthesis genes increases ecological fitness of cyanophage in silico. Environ. Microbiol. 11, 1386–1394 (2009).

    CAS  PubMed  Google Scholar 

  94. Bragg, J. G. & Chisholm, S. W. Modeling the fitness consequences of a cyanophage-encoded photosynthesis gene. PLOS ONE 3, e3550 (2008).

    PubMed  PubMed Central  Google Scholar 

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

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  97. Brown, C. M. & Bidle, K. D. Attenuation of virus production at high multiplicities of infection in Aureococcus anophagefferens. Virology 466–467, 71–81 (2014).

    PubMed  Google Scholar 

  98. Waters, R. E. & Chan, A. T. Micromonas pusilla virus: the virus growth cycle and associated physiological events within the host cells; host range mutation. J. Gen. Virol. 63, 199–206 (1982).

    Google Scholar 

  99. Allen, M. J., Schroeder, D. C., Donkin, A., Crawfurd, K. J. & Wilson, W. H. Genome comparison of two coccolithoviruses. Virol. J. 3, 15 (2006).

    PubMed  PubMed Central  Google Scholar 

  100. Abrahão, J. et al. Tailed giant Tupanvirus possesses the most complete translational apparatus of the known virosphere. Nat. Commun. 9, 749 (2018).

    PubMed  PubMed Central  Google Scholar 

  101. Fischer, M. G., Allen, M. J., Wilson, W. H. & Suttle, C. A. Giant virus with a remarkable complement of genes infects marine zooplankton. Proc. Natl Acad. Sci. USA 107, 19508–19513 (2010).

  102. Schvarcz, C. R. & Steward, G. F. A giant virus infecting green algae encodes key fermentation genes. Virology 518, 423–433 (2018).

    CAS  PubMed  Google Scholar 

  103. Yutin, N. & Koonin, E. V. Proteorhodopsin genes in giant viruses. Biol. Direct 7, 34 (2012).

    CAS  PubMed  PubMed Central  Google Scholar 

  104. Pushkarev, A. et al. A distinct abundant group of microbial rhodopsins discovered using functional metagenomics. Nature 558, 595–599 (2018).

    CAS  PubMed  Google Scholar 

  105. Sharma, A. K., Spudich, J. L. & Doolittle, W. F. Microbial rhodopsins: functional versatility and genetic mobility. Trends Microbiol. 14, 463–469 (2006).

    CAS  PubMed  Google Scholar 

  106. Fuhrman, J. A., Schwalbach, M. S. & Stingl, U. Proteorhodopsins: an array of physiological roles? Nat. Rev. Microbiol. 6, 488–494 (2008).

    CAS  PubMed  Google Scholar 

  107. Shah, V., Chang, B. X. & Morris, R. M. Cultivation of a chemoautotroph from the SUP05 clade of marine bacteria that produces nitrite and consumes ammonium. ISME J. 11, 263–271 (2017).

    CAS  PubMed  Google Scholar 

  108. Anantharaman, K. et al. Sulfur oxidation genes in diverse deep-sea viruses. Science 344, 757–760 (2014).

    CAS  PubMed  Google Scholar 

  109. 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  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  111. Ahlgren, N. A., Fuchsman, C. A., Rocap, G. & Fuhrman, J. A. Discovery of several novel, widespread, and ecologically distinct marine Thaumarchaeota viruses that encode amoC nitrification genes. ISME J. 13, 618–631 (2018).

    PubMed  PubMed Central  Google Scholar 

  112. Clokie, M. R. J. & Mann, N. H. Marine cyanophages and light. Environ. Microbiol. 8, 2074–2082 (2006).

    CAS  PubMed  Google Scholar 

  113. Ni, T. & Zeng, Q. Diel infection of cyanobacteria by cyanophages. Front. Mar. Sci. 2, 123 (2016).

    Google Scholar 

  114. Cseke, C. S. & Farkas, G. L. Effect of light on the attachment of cyanophage AS-1 to Anacystis nidulans. J. Bacteriol. 137, 667–669 (1979).

    CAS  PubMed  PubMed Central  Google Scholar 

  115. Kao, C. C., Green, S., Stein, B. & Golden, S. S. Diel infection of a cyanobacterium by a contractile bacteriophage. Appl. Environ. Microbiol. 71, 4276–4279 (2005).

    CAS  PubMed  PubMed Central  Google Scholar 

  116. Jia, Y., Shan, J., Millard, A., Clokie, M. R. J. & Mann, N. H. Light-dependent adsorption of photosynthetic cyanophages to Synechococcus sp. WH7803. FEMS Microbiol. Lett. 310, 120–126 (2010).

    CAS  PubMed  Google Scholar 

  117. Reimers, A.-M., Knoop, H., Bockmayr, A. & Steuer, R. Cellular trade-offs and optimal resource allocation during cyanobacterial diurnal growth. Proc. Natl Acad. Sci. USA 114, E6457–E6465 (2017).

    CAS  PubMed  Google Scholar 

  118. Sheyn, U., Rosenwasser, S., Ben-Dor, S., Porat, Z. & Vardi, A. Modulation of host ROS metabolism is essential for viral infection of a bloom-forming coccolithophore in the ocean. ISME J. 10, 1742–1754 (2016).

    CAS  PubMed  PubMed Central  Google Scholar 

  119. Suttle, C. A. & Chen, F. Mechanisms and rates of decay of marine viruses in seawater. Appl. Environ. Microbiol. 58, 3721–3729 (1992).

    CAS  PubMed  PubMed Central  Google Scholar 

  120. Luo, E., Aylward, F. O., Mende, D. R. & Delong, E. F. Bacteriophage distributions and temporal variability in the ocean’s interior. mBio 8, e01903–e01917 (2017).

    CAS  PubMed  PubMed Central  Google Scholar 

  121. Kimura, S. et al. Diurnal infection patterns and impact of Microcystis cyanophages in a Japanese pond. Appl. Environ. Microbiol. 78, 5805–5811 (2012).

    CAS  PubMed  PubMed Central  Google Scholar 

  122. Yoshida, T. et al. Locality and diel cycling of viral production revealed by a 24 h time course cross-omics analysis in a coastal region of Japan. ISME J. 12, 1287–1295 (2018).

    CAS  PubMed  PubMed Central  Google Scholar 

  123. Liu, R., Liu, Y., Chen, Y., Zhan, Y. & Zeng, Q. Cyanobacterial viruses exhibit diurnal rhythms during infection. Proc. Natl Acad. Sci. USA 116, 14077–14082 (2019). This paper shows distinct diel-dependent life history traits in three Prochlorococcus phages, and that rhythmic phage transcription is linked to the photosynthetic activity of the host.

    CAS  PubMed  Google Scholar 

  124. Bremer, H. et al. Escherichia Coli and Salmonella: Cellular and Molecular Biology 2nd edn Vol. 2 (eds Neidhardt, F. C. et al.) 1553–1569 (ASM Press, 1996).

  125. Kirchman, D. L. Processes in Microbial Ecology 19–34 (Oxford Univ. Press, 2012).

  126. 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).

    CAS  PubMed  Google Scholar 

  127. Clasen, J. L. & Elser, J. J. The effect of host Chlorella NC64A carbon:phosphorus ratio on the production of Paramecium bursaria Chlorella Virus-1. Freshw. Biol. 52, 112–122 (2007).

    CAS  Google Scholar 

  128. Brown, C. M., Lawrence, J. E. & Campbell, D. A. Are phytoplankton population density maxima predictable through analysis of host and viral genomic DNA content? J. Mar. Biol. Assoc. UK 86, 491–498 (2006).

    CAS  Google Scholar 

  129. Edwards, K. F. & Steward, G. F. Host traits drive viral life histories across phytoplankton viruses. Am. Nat. 191, 566–581 (2018).

    PubMed  Google Scholar 

  130. 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).

    CAS  Google Scholar 

  131. Kozloff, L. M. & Putnam, F. W. Biochemical studies of virus reproduction: III. The origin of virus phosphorus in the Escherichia coli T6 bacteriophage system. J. Biol. Chem. 182, 229–242 (1950).

    CAS  Google Scholar 

  132. Pasulka, A. L. et al. Interrogating marine virus–host interactions and elemental transfer with BONCAT and nanoSIMS-based methods. Environ. Microbiol. 20, 671–692 (2018).

    CAS  PubMed  Google Scholar 

  133. Stent, G. S. & Maaløe, O. Radioactive phosphorus tracer studies on the reproduction of T4 bacteriophage. Biochim. Biophys. Acta 10, 55–69 (1953).

    CAS  PubMed  Google Scholar 

  134. 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).

    CAS  PubMed  PubMed Central  Google Scholar 

  135. 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).

    CAS  PubMed  Google Scholar 

  136. Tetu, S. G. et al. Microarray analysis of phosphate regulation in the marine cyanobacterium Synechococcus sp. WH8102. ISME J. 3, 835–849 (2009).

    CAS  PubMed  Google Scholar 

  137. 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).

    CAS  PubMed  PubMed Central  Google Scholar 

  138. Bertilsson, S., Berglund, O., Karl, D. M. & Chisholm, S. W. Elemental composition of marine Prochlorococcus and Synechococcus: implications for the ecological stoichiometry of the sea. Limnol. Oceanogr. 48, 1721–1731 (2003).

    CAS  Google Scholar 

  139. Martiny, A. C., Coleman, M. L. & Chisholm, S. W. Phosphate acquisition genes in Prochlorococcus ecotypes: evidence for genome-wide adaptation. Proc. Natl Acad. Sci. USA 103, 12552–12557 (2006).

    CAS  PubMed  Google Scholar 

  140. Wilson, W. H. et al. Complete genome sequence and lytic phase transcription profile of a Coccolithovirus. Science 309, 1090–1092 (2005).

    CAS  PubMed  Google Scholar 

  141. Monier, A. et al. Host-derived viral transporter protein for nitrogen uptake in infected marine phytoplankton. Proc. Natl Acad. Sci. USA 114, E7489–E7498 (2017). This study reports the first nitrogen transport gene in an algal virus isolate and shows that it enables uptake of ammonium as well as organic nitrogen substrates.

    CAS  PubMed  Google Scholar 

  142. Monier, A. et al. Phosphate transporters in marine phytoplankton and their viruses: cross-domain commonalities in viral–host gene exchanges. Environ. Microbiol. 14, 162–176 (2012).

    CAS  PubMed  PubMed Central  Google Scholar 

  143. Grossman, A. R., Schaefer, M. R., Chiang, G. G. & Collier, J. L. The phycobilisome, a light-harvesting complex responsive to environmental conditions. Microbiol. Rev. 57, 725–749 (1993).

    CAS  PubMed  PubMed Central  Google Scholar 

  144. Gao, E.-B., Gui, J.-F. & Zhang, Q.-Y. A novel cyanophage with a cyanobacterial nonbleaching protein A gene in the genome. J. Virol. 86, 236–245 (2012).

    CAS  PubMed  PubMed Central  Google Scholar 

  145. Ou, T., Gao, X. C., Li, S. H. & Zhang, Q. Y. Genome analysis and gene nblA identification of Microcystis aeruginosa myovirus (MaMV-DC) reveal the evidence for horizontal gene transfer events between cyanomyovirus and host. J. Gen. Virol. 96, 3681–3697 (2015).

    CAS  PubMed  Google Scholar 

  146. Nadel, O. et al. Uncultured marine cyanophages encode for active NblA, phycobilisome proteolysis adaptor protein. Preprint at bioRxiv https://doi.org/10.1101/494369 (2018).

  147. Ma, X., Coleman, M. L. & Waldbauer, J. R. Distinct molecular signatures in dissolved organic matter produced by viral lysis of marine cyanobacteria. Environ. Microbiol. 20, 3001–3011 (2018).

    CAS  PubMed  Google Scholar 

  148. Sañudo-Wilhelmy, S. A. et al. Multiple B-vitamin depletion in large areas of the coastal ocean. Proc. Natl Acad. Sci. USA 109, 14041–14045 (2012).

    PubMed  Google Scholar 

  149. Croft, M. T., Lawrence, A. D., Raux-Deery, E., Warren, M. J. & Smith, A. G. Algae acquire vitamin B12 through a symbiotic relationship with bacteria. Nature 438, 90–93 (2005).

    CAS  PubMed  Google Scholar 

  150. Heal, K. R. et al. Two distinct pools of B12 analogs reveal community interdependencies in the ocean. Proc. Natl Acad. Sci. USA 114, 364–369 (2017).

    CAS  PubMed  Google Scholar 

  151. López-Pérez, M., Haro-Moreno, J. M., de la Torre, J. R. & Rodriguez-Valera, F. Novel caudovirales associated with Marine Group I Thaumarchaeota assembled from metagenomes. Environ. Microbiol. 21, 1980–1988 (2019).

    PubMed  Google Scholar 

  152. Ignacio-Espinoza, J. C. & Sullivan, M. B. Phylogenomics of T4 cyanophages: lateral gene transfer in the ‘core’ and origins of host genes. Environ. Microbiol. 14, 2113–2126 (2012).

    CAS  PubMed  Google Scholar 

  153. Moore, J. K., Doney, S. C. & Lindsay, K. Upper ocean ecosystem dynamics and iron cycling in a global three-dimensional model. Glob. Biogeochem. Cycles 18, GB4028 (2004).

    Google Scholar 

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

    Google Scholar 

  155. Gledhill, M. et al. Effect of metals on the lytic cycle of the coccolithovirus, EhV86. Front. Microbiol. 3, 155 (2012).

    PubMed  PubMed Central  Google Scholar 

  156. Gasper, R. et al. Distinct features of cyanophage-encoded T-type phycobiliprotein lyase ΦCpeT: the role of auxiliary metabolic genes. J. Biol. Chem. 292, 3089–3098 (2017).

    CAS  PubMed  PubMed Central  Google Scholar 

  157. Nissimov, J. I. et al. Biochemical diversity of glycosphingolipid biosynthesis as a driver of Coccolithovirus competitive ecology. Environ. Microbiol. 21, 2182–2197 (2019).

    CAS  PubMed  Google Scholar 

  158. Deng, L. et al. Grazing of heterotrophic flagellates on viruses is driven by feeding behaviour. Environ. Microbiol. Rep. 6, 325–330 (2014).

    CAS  PubMed  Google Scholar 

  159. Baltar, F. Watch out for the ‘living dead’: cell-free enzymes and their fate. Front. Microbiol. 8, 2438 (2018).

    PubMed  PubMed Central  Google Scholar 

  160. Malits, A., Christaki, U., Obernosterer, I. & Weinbauer, M. G. Enhanced viral production and virus-mediated mortality of bacterioplankton in a natural iron-fertilized bloom event above the kerguelen plateau. Biogeosciences 11, 6841–6853 (2014).

    Google Scholar 

  161. Motegi, C. et al. Viral control of bacterial growth efficiency in marine pelagic environments. Limnol. Oceanogr. 54, 1901–1910 (2009).

    CAS  Google Scholar 

  162. 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).

    CAS  PubMed  Google Scholar 

  163. 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  Google Scholar 

  164. Talmy, D. et al. An empirical model of carbon flow through marine viruses and microzooplankton grazers. Environ. Microbiol. 21, 2171–2181 (2019). Using an empirically parameterized model constrained by estimates of prey, predator and viral life history traits, this study calculates carbon flows from primary producers to viruses, grazers and lysates in a marine ecosystem.

    CAS  PubMed  Google Scholar 

  165. Lønborg, C., Middelboe, M. & Brussaard, C. P. D. Viral lysis of Micromonas pusilla: impacts on dissolved organic matter production and composition. Biogeochemistry 116, 231–240 (2013).

    Google Scholar 

  166. Lelchat, F. et al. Viral degradation of marine bacterial exopolysaccharides. FEMS Microbiol. Ecol. 95, fiz079 (2019).

    CAS  PubMed  Google Scholar 

  167. Middelboe, M. & Jørgensen, N. O. G. Viral lysis of bacteria: an important source of dissolved amino acids and cell wall compounds. J. Mar. Biol. Assoc. UK 86, 605–612 (2006).

    CAS  Google Scholar 

  168. Yamada, Y., Tomaru, Y., Fukuda, H. & Nagata, T. Aggregate formation during the viral lysis of a marine diatom. Front. Mar. Sci. 5, 167 (2018).

    Google Scholar 

  169. 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).

    Google Scholar 

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

    CAS  Google Scholar 

  171. Gobler, C. J., Hutchins, D. A., Fisher, N. S., Cosper, E. M. & Sanudo-Wilhelmy, S. A. Release and bioavailability of C, N, P, Se, and Fe following viral lysis of a marine chrysophyte. Limnol. Oceanogr. 42, 1492–1504 (1997).

    CAS  Google Scholar 

  172. Middelboe, M., Jørgensen, N. O. G. & Kroer, N. Effects of viruses on nutrient turnover and growth efficiency of noninfected marine bacterioplankton. Appl. Environ. Microbiol. 62, 1991–1997 (1996).

    CAS  PubMed  PubMed Central  Google Scholar 

  173. Jiao, N. et al. Microbial production of recalcitrant dissolved organic matter: long-term carbon storage in the global ocean. Nat. Rev. Microbiol. 8, 593–599 (2010).

    CAS  PubMed  Google Scholar 

  174. Moreno, A. R. & Martiny, A. C. Ecological stoichiometry of ocean plankton. Ann. Rev. Mar. Sci. 10, 43–69 (2018).

    PubMed  Google Scholar 

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

    PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  177. Laber, C. P. et al. Coccolithovirus facilitation of carbon export in the North Atlantic. Nat. Microbiol. 3, 537–547 (2018). This field study marshals an array of evidence to provide some of the first direct measurements of the effects of viral infection on large-scale carbon export in a natural marine ecosystem.

    CAS  PubMed  Google Scholar 

  178. Johns, C. T. et al. The mutual interplay between calcification and coccolithovirus infection. Environ. Microbiol. 21, 1896–1915 (2019).

    CAS  PubMed  Google Scholar 

  179. Evans, C. & Wilson, W. H. Preferential grazing of Oxyrrhis marina on virus-infected Emiliania huxleyi. Limnol. Oceanogr. 53, 2035–2040 (2008).

    Google Scholar 

  180. Vermont, A. I. et al. Virus infection of Emiliania huxleyi deters grazing by the copepod Acartia tonsa. J. Plankton Res. 38, 1194–1205 (2016).

    Google Scholar 

  181. Frada, M. J. et al. Zooplankton may serve as transmission vectors for viruses infecting algal blooms in the ocean. Curr. Biol. 24, 2592–2597 (2014).

    CAS  PubMed  Google Scholar 

  182. Lawrence, J. et al. Viruses on the menu: the appendicularian Oikopleura dioica efficiently removes viruses from seawater. Limnol. Oceanogr. 63, S244–S253 (2018).

    Google Scholar 

  183. Gonzalez, J. M. & Suttle, C. A. Grazing by marine nanoflagellates on viruses and virus-sized particles: ingestion and digestion. Mar. Ecol. Prog. Ser. 94, 1–10 (1993).

    Google Scholar 

  184. Record, N. R., Talmy, D. & Våge, S. Quantifying tradeoffs for marine viruses. Front. Mar. Sci. 3, 251 (2016).

    Google Scholar 

  185. Mateus, M. D. Bridging the gap between knowing and modeling viruses in marine systems — an upcoming frontier. Front. Mar. Sci. 3, 284 (2017).

    Google Scholar 

  186. Intergovernmental Panel on Climate Change. Climate Change 2014: synthesis report. Contribution of Working Groups I, II and III to the fifth assessment report of the Intergovernmental Panel on Climate Change (IPCC, 2014).

  187. Stocker, T. F. et al. Climate Change 2013 — The Physical Science Basis (Cambridge Univ. Press, 2014).

  188. Stock, C. A., Dunne, J. P. & John, J. G. Global-scale carbon and energy flows through the marine planktonic food web: an analysis with a coupled physical–biological model. Prog. Oceanogr. 120, 1–28 (2014).

    Google Scholar 

  189. Aumont, O., Ethé, C., Tagliabue, A., Bopp, L. & Gehlen, M. PISCES-v2: an ocean biogeochemical model for carbon and ecosystem studies. Geosci. Model. Dev. 8, 2465–2513 (2015).

    CAS  Google Scholar 

  190. Danovaro, R. et al. Marine viruses and global climate change. FEMS Microbiol. Rev. 35, 993–1034 (2011).

    CAS  PubMed  Google Scholar 

  191. Nissimov, J. I., Napier, J. A., Allen, M. J. & Kimmance, S. A. Intragenus competition between coccolithoviruses: an insight on how a select few can come to dominate many. Environ. Microbiol. 18, 133–145 (2016).

    CAS  PubMed  Google Scholar 

  192. Zimmerman, A. E. et al. Closely related viruses of the marine picoeukaryotic alga Ostreococcus lucimarinus exhibit different ecological strategies. Environ. Microbiol. 21, 2148–2170 (2019).

    PubMed  PubMed Central  Google Scholar 

  193. Martiny, A. C. et al. Strong latitudinal patterns in the elemental ratios of marine plankton and organic matter. Nat. Geosci. 6, 279–283 (2013).

    CAS  Google Scholar 

  194. Weber, T. S. & Deutsch, C. Ocean nutrient ratios governed by plankton biogeography. Nature 467, 550–554 (2010).

    CAS  PubMed  Google Scholar 

  195. Weitz, J. S., Li, G., Gulbudak, H., Cortez, M. H. & Whitaker, R. J. Viral invasion fitness across a continuum from lysis to latency. Virus Evol. 5, vez006 (2019).

    PubMed  PubMed Central  Google Scholar 

  196. Mai-Prochnow, A. et al. ‘Big things in small packages: the genetics of filamentous phage and effects on fitness of their host’. FEMS Microbiol. Rev. 39, 465–487 (2015).

    PubMed  Google Scholar 

  197. Brüssow, H., Canchaya, C. & Hardt, W.-D. Phages and the evolution of bacterial pathogens: from genomic rearrangements to lysogenic conversion. Microbiol. Mol. Biol. Rev. 68, 560–602 (2004).

    PubMed  PubMed Central  Google Scholar 

  198. Obeng, N., Pratama, A. A. & Elsas, J. D. van. The significance of mutualistic phages for bacterial ecology and evolution. Trends Microbiol. 24, 440–449 (2016).

    CAS  PubMed  Google Scholar 

  199. Feiner, R. et al. A new perspective on lysogeny: prophages as active regulatory switches of bacteria. Nat. Rev. Microbiol. 13, 641–650 (2015).

    CAS  PubMed  Google Scholar 

  200. Choua, M. & Bonachela, J. A. Ecological and evolutionary consequences of viral plasticity. Am. Nat. 193, 346–358 (2019).

    PubMed  Google Scholar 

  201. Dang, V. T., Howard-Varona, C., Schwenck, S. & Sullivan, M. B. Variably lytic infection dynamics of large Bacteroidetes podovirus phi38:1 against two Cellulophaga baltica host strains. Environ. Microbiol. 17, 4659–4671 (2015).

    CAS  PubMed  Google Scholar 

  202. Bryan, D., El-Shibiny, A., Hobbs, Z., Porter, J. & Kutter, E. M. Bacteriophage T4 infection of stationary phase E. coli: life after log from a phage perspective. Front. Microbiol. 7, 1391 (2016).

    PubMed  PubMed Central  Google Scholar 

  203. Mackinder, L. C. M. et al. A unicellular algal virus, Emiliania huxleyi virus 86, exploits an animal-like infection strategy. J. Gen. Virol. 90, 2306–2316 (2009).

    CAS  PubMed  Google Scholar 

  204. Thomas, R. et al. Acquisition and maintenance of resistance to viruses in eukaryotic phytoplankton populations. Environ. Microbiol. 13, 1412–1420 (2011).

    PubMed  Google Scholar 

  205. Adams, M. H. Bacteriophages (Interscience, 1959).

  206. Hyman, P. & Abedon, S. T. in Bacteriophages. Methods and Protocols, Volume 1: Isolation, Characterization, and Interaction (eds Clokie, M. R. J. & Kropinski, A. M.) 175–202 (Humana Press, 2009).

  207. Abedon, S. T. Phage therapy dosing: the problem(s) with multiplicity of infection (MOI). Bacteriophage 6, e1220348 (2016).

    PubMed  PubMed Central  Google Scholar 

  208. Mayer, J. A. & Taylor, F. J. R. A virus which lyses the marine nanoflagellate Micromonas pusilla. Nature 281, 299–301 (1979).

    Google Scholar 

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

    CAS  PubMed  Google Scholar 

  210. Reistetter, E. N. et al. Effects of phosphorus starvation versus limitation on the marine cyanobacterium Prochlorococcus MED4 II: gene expression. Environ. Microbiol. 15, 2129–2143 (2013).

    CAS  PubMed  Google Scholar 

  211. Guo, J. et al. Specialized proteomic responses and an ancient photoprotection mechanism sustain marine green algal growth during phosphate limitation. Nat. Microbiol. 3, 781–790 (2018).

    CAS  PubMed  Google Scholar 

  212. Gerringa, L. J. A., de Baar, H. J. W. & Timmermans, K. R. A comparison of iron limitation of phytoplankton in natural oceanic waters and laboratory media conditioned with EDTA. Mar. Chem. 68, 335–346 (2000).

    CAS  Google Scholar 

  213. Mistry, B. A., D’Orsogna, M. R. & Chou, T. The effects of statistical multiplicity of infection on virus quantification and infectivity assays. Biophys. J. 114, 2974–2985 (2018).

    CAS  PubMed  PubMed Central  Google Scholar 

  214. Kirzner, S., Barak, E. & Lindell, D. Variability in progeny production and virulence of cyanophages determined at the single-cell level. Environ. Microbiol. Rep. 8, 605–613 (2016).

    PubMed  Google Scholar 

  215. Cheng, Y. S., Labavitch, J. & VanderGheynst, J. S. Organic and inorganic nitrogen impact Chlorella variabilis productivity and host quality for viral production and cell lysis. Appl. Biochem. Biotechnol. 176, 467–479 (2015).

    CAS  PubMed  Google Scholar 

  216. Maat, D. S., Crawfurd, K. J., Timmermans, K. R. & Brussaard, C. P. D. Elevated CO2 and phosphate limitation favor Micromonas pusilla through stimulated growth and reduced viral impact. Appl. Environ. Microbiol. 80, 3119–3127 (2014).

    PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

This work was supported by the Gordon & Betty Moore Foundation Marine Microbiology Initiative (Award 3305). Additional support was provided by the National Science Foundation Division of Ocean Sciences (NSF-OCE) (Awards 1536989 and 1829831 to M.B.S.), the Simons Foundation (Awards 32910 to S.J. and 402971 to J.R.W.) and the Gordon & Betty Moore Foundation (Awards 3788 to A.Z.W. and 3790 to M.B.S.).

Author information

Authors and Affiliations

  1. Department of the Geophysical Sciences, University of Chicago, Chicago, IL, USA

    Amy E. Zimmerman, Jacob R. Waldbauer & Maureen L. Coleman

  2. Department of Microbiology, Ohio State University, Columbus, OH, USA

    Cristina Howard-Varona & Matthew B. Sullivan

  3. Monterey Bay Aquarium Research Institute, Moss Landing, CA, USA

    David M. Needham & Alexandra Z. Worden

  4. Department of Earth Science, University of Southern California, Los Angeles, CA, USA

    Seth G. John

  5. Ocean EcoSystems Biology Unit, GEOMAR Helmholtz Centre for Ocean Research Kiel, Kiel, Germany

    Alexandra Z. Worden

  6. Department of Civil, Environmental and Geodetic Engineering, Ohio State University, Columbus, OH, USA

    Matthew B. Sullivan

Authors
  1. Amy E. Zimmerman
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Cristina Howard-Varona
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. David M. Needham
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Seth G. John
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Alexandra Z. Worden
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Matthew B. Sullivan
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Jacob R. Waldbauer
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Maureen L. Coleman
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

All authors contributed to the conception, research, writing and editing of the article.

Corresponding author

Correspondence to Maureen L. Coleman.

Ethics declarations

Competing interests

The authors declare no competing interests.

Additional information

Peer review information

Nature Reviews Microbiology thanks K. Bidle and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary information

Glossary

Transparent exopolymer particle

(TEP). A sticky, gel-like particle consisting predominantly of acidic polysaccharides that originate from microorganisms and can enhance the aggregation of non-sticky particles in marine and aquatic ecosystems.

Core reaction centre

A membrane complex of several proteins, pigments and other cofactors that performs the principal energy conversion reactions of photosynthesis, capturing light energy and converting it into redox potential energy for ATP synthesis and reducing power for reduction of CO2; also known as the photosynthetic reaction centre.

Phycobilin

Photosynthetic pigments found in cyanobacteria and the chloroplasts of red algae and glaucophytes that aid in absorption of light energy, particularly at wavelengths that are not well absorbed by chlorophylls or carotenoids.

Euphotic zone

The uppermost layer of water in a lake or ocean characterized by enough sunlight to support photosynthetic carbon fixation.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zimmerman, A.E., Howard-Varona, C., Needham, D.M. et al. Metabolic and biogeochemical consequences of viral infection in aquatic ecosystems. Nat Rev Microbiol 18, 21–34 (2020). https://doi.org/10.1038/s41579-019-0270-x

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/s41579-019-0270-x

This article is cited by

Search

Advanced search

Quick links

Nature Briefing Microbiology

Sign up for the Nature Briefing: Microbiology newsletter — what matters in microbiology research, free to your inbox weekly.

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