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Prochlorococcus viruses—From biodiversity to biogeochemical cycles

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Abstract

As the dominant primary producer in oligotrophic oceans, the unicellular picocyanobacterium Prochlorococcus is the smallest and most abundant photosynthetic phytoplankton in the world and plays an important role in marine carbon cycling. Cyanophages that infect Prochlorococcus influence the growth, carbon fixation, diversity, evolution, and environmental adaptation of their hosts. Here, we review studies on the isolation, genomics, and phylogenetic diversity of Prochlorococcus viruses and their interactions with Prochlorococcus. We also review the potential effects of Prochlorococcus viruses on biogeochemical cycling in the ocean.

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References

  • Allen L Z, Ishoey T, Novotny M A, McLean J S, Lasken R S, Williamson S J. 2011. Single virus genomics: A new tool for virus discovery. Plos One, 6: e17722

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Avrani S, Lindell D. 2015. Convergent evolution toward an improved growth rate and a reduced resistance range in Prochlorococcus strains resistant to phage. Proc Natl Acad Sci USA, 112: E2191–E2200

    Article  Google Scholar 

  • Baudoux A C, Veldhuis M J W, Witte H J, Brussaard C P D. 2007. Viruses as mortality agents of picophytoplankton in the deep chlorophyll maximum layer during IRONAGES III. Limnol Oceanogr, 52: 2519–2529

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Biller S J, Berube P M, Lindell D, Chisholm S W. 2015. Prochlorococcus: The structure and function of collective diversity. Nat Rev Microbiol, 13: 13–27

    Article  Google Scholar 

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

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Campbell L, Liu H, Nolla H A, Vaulot D. 1997. Annual variability of phytoplankton and bacteria in the subtropical North Pacific Ocean at Station ALOHA during the 1991–1994 ENSO event. Deep-Sea Res Part I-Oceanogr Res Pap, 44: 167–192

    Article  Google Scholar 

  • Chisholm S W, Olson R J, Zettler E R, Goericke R, Waterbury J B, Welschmeyer N A. 1988. A novel free-living prochlorophyte abundant in the oceanic euphotic zone. Nature, 334: 340–343

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Dekel-Bird N P, Avrani S, Sabehi G, Pekarsky I, Marston M F, Kirzner S, Lindell D. 2013. Diversity and evolutionary relationships of T7-like podoviruses infecting marine cyanobacteria. Environ Microbiol, 15: 1476–1491

    Article  Google Scholar 

  • Doron S, Fedida A, Hernández-Prieto M A, Sabehi G, Karunker I, Stazic D, Feingersch R, Steglich C, Futschik M, Lindell D, Sorek R. 2016. Transcriptome dynamics of a broad host-range cyanophage and its hosts. ISME J, 10: 1437–1455

    Article  Google Scholar 

  • Enav H, Béjà O, Mandel-Gutfreund Y. 2012. Cyanophage tRNAs may have a role in cross-infectivity of oceanic Prochlorococcus and Synechococcus hosts. ISME J, 6: 619–628

    Article  Google Scholar 

  • Flombaum P, Gallegos J L, Gordillo R A, Rincón J, Zabala L L, Jiao N Z, Karl D M, Li W K W, Lomas M W, Veneziano D, Vera C S, Vrugt J A, Martiny A C. 2013. Present and future global distributions of the marine Cyanobacteria Prochlorococcus and Synechococcus. Proc Natl Acad Sci USA, 110: 9824–9829

    Article  Google Scholar 

  • Fridman S, Flores-Uribe J, Larom S, Alalouf O, Liran O, Yacoby I, Salama F, Bailleul B, Rappaport F, Ziv T, Sharon I, Cornejo-Castillo F M, Philosof A, Dupont C L, Sánchez P, Acinas S G, Rohwer F L, Lindell D, Béjà O. 2017. A myovirus encoding both photosystem I and II proteins enhances cyclic electron flow in infected Prochlorococcus cells. Nat Microbiol, 2: 1350–1357

    Article  Google Scholar 

  • Fuhrman J A. 1999. Marine viruses and their biogeochemical and ecological effects. Nature, 399: 541–548

    Article  Google Scholar 

  • Gérikas-Ribeiro C, Dos Santos A L, Marie D, Helena Pellizari V, Pereira Brandini F, Vaulot D. 2016. Pico and nanoplankton abundance and carbon stocks along the Brazilian Bight. Peer J, 4: e2587

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Goericke R, Welschmeyer N A. 1993. The marine prochlorophyte Prochlorococcus contributes significantly to phytoplankton biomass and primary production in the Sargasso Sea. Deep-Sea Res Part I-Oceanogr Res Pap, 40: 2283–2294

    Article  Google Scholar 

  • Heldal M, Scanlan D J, Norland S, Thingstad F, Mann N H. 2003. Elemental composition of single cells of various strains of marine Prochlorococcus and Synechococcus using X-ray microanalysis. Limnol Oceanogr, 48: 1732–1743

    Article  Google Scholar 

  • Hevroni G, Enav H, Rohwer F, Béjà O. 2015. Diversity of viral photosystem- I psaA genes. ISME J, 9: 1892–1898

    Article  Google Scholar 

  • Huang S, Zhang S, Jiao N, Chen F. 2015. Marine cyanophages demonstrate biogeographic patterns throughout the global ocean. Appl Environ Microbiol, 81: 441–452

    Article  Google Scholar 

  • Jiao N Z, Yang Y H. 2002. Ecological studies on Prochlorococcus in China seas. Chin Sci Bull, 47: 1243–1250

    Article  Google Scholar 

  • Jiao N Z, Herndl G J, Hansell D A, Benner R, Kattner G, Wilhelm S W, Kirchman D L, Weinbauer M G, Luo T W, Chen F, Azam F. 2010. Microbial production of recalcitrant dissolved organic matter: Longterm carbon storage in the global ocean. Nat Rev Microbiol, 8: 593–599

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Kashtan N, Roggensack S E, Rodrigue S, Thompson J W, Biller S J, Coe A, Ding H, Marttinen P, Malmstrom R R, Stocker R, Follows M J, Stepanauskas R, Chisholm S W. 2014. Single-cell genomics reveals hundreds of coexisting subpopulations in wild Prochlorococcus. Science, 344: 416–420

    Article  Google Scholar 

  • Kashtan N, Roggensack S E, Berta-Thompson J W, Grinberg M, Stepanauskas R, Chisholm S W. 2017. Fundamental differences in diversity and genomic population structure between Atlantic and Pacific Prochlorococcus. ISME J, 11: 1997–2011

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Kent A G, Dupont C L, Yooseph S, Martiny A C. 2016. Global biogeography of Prochlorococcus genome diversity in the surface ocean. ISME J, 10: 1856–1865

    Article  Google Scholar 

  • Labrie S J, Frois-Moniz K, Osburne M S, Kelly L, Roggensack S E, Sullivan M B, Gearin G, Zeng Q, Fitzgerald M, Henn M R, Chisholm S W. 2013. Genomes of marine cyanopodoviruses reveal multiple origins of diversity. Environ Microbiol, 15: 1356–1376

    Article  Google Scholar 

  • Lin X Q, Ding H M, Zeng Q L. 2016. Transcriptomic response during phage infection of a marine cyanobacterium under phosphorus-limited conditions. Environ Microbiol, 18: 450–460

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Lindell D, Jaffe J D, Coleman M L, Futschik M E, Axmann I M, Rector T, Kettler G, Sullivan M B, Steen R, Hess W R, Church G M, Chisholm S W. 2007. Genome-wide expression dynamics of a marine virus and host reveal features of co-evolution. Nature, 449: 83–86

    Article  Google Scholar 

  • Liu H B, Nolla H, Campbell L. 1997. Prochlorococcus growth rate and contribution to primary production in the equatorial and subtropical North Pacific Ocean. Aquat Microb Ecol, 12: 39–47

    Article  Google Scholar 

  • Middelboe M, Jørgensen N O G. 2006. Viral lysis of bacteria: An important source of dissolved amino acids and cell wall compounds. J Mar Biol Ass, 86: 605–612

    Article  Google Scholar 

  • Mojica K D A, Huisman J, Wilhelm S W, Brussaard C P D. 2016. Latitudinal variation in virus-induced mortality of phytoplankton across the North Atlantic Ocean. ISME J, 10: 500–513

    Article  Google Scholar 

  • Moore L R, Coe A, Zinser E R, Saito M A, Sullivan M B, Lindell D, Frois-Moniz K, Waterbury J, Chisholm S W. 2007. Culturing the marine cyanobacterium Prochlorococcus. Limnol Oceanogr Methods, 5: 353–362

    Article  Google Scholar 

  • Morris J J, Kirkegaard R, Szul M J, Johnson Z I, Zinser E R. 2008. Facilitation of robust growth of Prochlorococcus colonies and dilute liquid cultures by “Helper” heterotrophic bacteria. Appl Environ Microbiol, 74: 4530–4534

    Article  Google Scholar 

  • Partensky F, Hess W R, Vaulot D. 1999. Prochlorococcus, a marine photosynthetic prokaryote of global significance. Microbiol Mol Biol Rev, 63: 106–127

    Google Scholar 

  • Partensky F, Garczarek L. 2010. Prochlorococcus: Advantages and Limits of Minimalism. Annu Rev Mar Sci, 2: 305–331

    Article  Google Scholar 

  • Pasulka A L, Samo T J, Landry M R. 2015. Grazer and viral impacts on microbial growth and mortality in the southern California Current Ecosystem. J Plankton Res, 37: 320–336

    Article  Google Scholar 

  • Paul J H, Sullivan M B, Segall A M, Rohwer F. 2002. Marine phage genomics. Comp Biochem Physiol Part B-Biochem Mol Biol, 133: 463–476

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Rohwer F, Edwards R. 2002. The phage proteomic tree: A genome-based taxonomy for phage. J Bacteriol, 184: 4529–4535

    Article  Google Scholar 

  • Rohwer F, Thurber R V. 2009. Viruses manipulate the marine environment. Nature, 459: 207–212

    Article  Google Scholar 

  • Sullivan M B, Waterbury J B, Chisholm S W. 2003. Erratum: Cyanophages infecting the oceanic cyanobacterium Prochlorococcus. Nature, 424: 1047–1051

    Article  Google Scholar 

  • Sullivan M B, Coleman M L, Weigele P, Rohwer F, Chisholm S W. 2005. Three Prochlorococcus cyanophage genomes: Signature features and ecological interpretations. PLoS Biol, 3: e144–806

    Article  Google Scholar 

  • Sullivan M B, Lindell D, Lee J A, Thompson L R, Bielawski J P, Chisholm S W. 2006. Prevalence and evolution of core photosystem II genes in marine cyanobacterial viruses and their hosts. Plos Biol, 4: e234

    Article  Google Scholar 

  • Sullivan M B, Krastins B, Hughes J L, Kelly L, Chase M, Sarracino D, Chisholm S W. 2009. The genome and structural proteome of an ocean siphovirus: A new window into the cyanobacterial ‘mobilome’. Environ Microbiol, 11: 2935–2951

    Article  Google Scholar 

  • Sullivan M B, Coleman M L, Quinlivan V, Rosenkrantz J E, Defrancesco A S, Tan G, Fu R, Lee J A, Waterbury J B, Bielawski J P, Chisholm S W. 2008. Portal protein diversity and phage ecology. Environ Microbiol, 10: 2810–2823

    Article  Google Scholar 

  • Sullivan M B, Huang K H, Ignacio-Espinoza J C, Berlin A M, Kelly L, Weigele P R, DeFrancesco A S, Kern S E, Thompson L R, Young S, Yandava C, Fu R, Krastins B, Chase M, Sarracino D, Osburne M S, Henn M R, Chisholm S W. 2010. Genomic analysis of oceanic cyanobacterial myoviruses compared with T4-like myoviruses from diverse hosts and environments. Environ Microbiol, 12: 3035–3056

    Article  Google Scholar 

  • Suttle C A. 2005. Viruses in the sea. Nature, 437: 356–361

    Article  Google Scholar 

  • Suttle C A. 2007. Marine viruses—Major players in the global ecosystem. Nat Rev Microbiol, 5: 801–812

    Article  Google Scholar 

  • Thompson L R, Zeng Q, Kelly L, Huang K H, Singer A U, Stubbe J, Chisholm S W. 2011. Phage auxiliary metabolic genes and the redirection of cyanobacterial host carbon metabolism. Proc Natl Acad Sci USA, 108: E757–E764

    Article  Google Scholar 

  • Vaulot D, Partensky F É É, Neveux J, Mantoura R F C, Llewellyn C A. 1990. Winter presence of prochlorophytes in surface waters of the northwestern Mediterranean Sea. Limnol Oceanogr, 35: 1156–1164

    Article  Google Scholar 

  • Waterbury J B, Valois F W. 1993. Resistance to cooccurring phages enables marine synechococcus communities to coexist with cyanophages abundant in seawater. Appl Environ Microbiol, 59: 3393–3399

    Google Scholar 

  • Wilhelm S W, Suttle C A. 1999. Viruses and nutrient cycles in the sea. Bioscience, 49: 781–788

    Article  Google Scholar 

  • Yang Y, Cai L, Ma R, Xu Y, Tong Y, Huang Y, Jiao N, Zhang R. 2017. A novel roseosiphophage isolated from the oligotrophic south china sea. Viruses, 9: 109

    Article  Google Scholar 

  • Zeng Q, Chisholm S W. 2012. Marine viruses exploit their host’s twocomponent regulatory system in response to resource limitation. Curr Biol, 22: 124–128

    Article  Google Scholar 

  • Zhang R, Wei W, Cai L L. 2014. The fate and biogeochemical cycling of viral elements. Nat Rev Microbiol, 12: 850–851

    Article  Google Scholar 

  • Zhao Z, Gonsior M, Luek J, Timko S, Ianiri H, Hertkorn N, Schmitt-Kopplin P, Fang X, Zeng Q, Jiao N, Chen F. 2017. Picocyanobacteria and deep-ocean fluorescent dissolved organic matter share similar optical properties. Nat Commun, 8: 15284

    Article  Google Scholar 

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Acknowledgements

This work was supported by the Qingdao National Laboratory for Marine Science and Technology (Grant No. QNLM2016ORP0303), and the National Natural Science Foundation of China (Grant Nos. 41522603 & 91428308), and the China National Offshore Oil Corporation (Grant Nos. CNOOC-KJ125FZDXM00TJ001-2014 & CNOOC-KJ125FZDXM00ZJ001-2014).

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Authors and Affiliations

  1. State Key Laboratory of Marine Environmental Science, College of Ocean & Earth Sciences, Institute of Marine Microbes and Ecospheres, Xiamen University, Xiamen, 361102, China

    Xilin Xiao, Rui Zhang & Nianzhi Jiao

  2. Department of Ocean Science and Division of Life Science, Hong Kong University of Science and Technology, Clear Water Bay, Hong Kong, 999077, China

    Qinglu Zeng

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  1. Xilin Xiao
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  2. Qinglu Zeng
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Correspondence to Rui Zhang or Nianzhi Jiao.

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Xiao, X., Zeng, Q., Zhang, R. et al. Prochlorococcus viruses—From biodiversity to biogeochemical cycles. Sci. China Earth Sci. 61, 1728–1736 (2018). https://doi.org/10.1007/s11430-017-9247-4

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