Advertisement

Science China Earth Sciences

, Volume 61, Issue 12, pp 1728–1736 | Cite as

Prochlorococcus viruses—From biodiversity to biogeochemical cycles

  • Xilin Xiao
  • Qinglu Zeng
  • Rui ZhangEmail author
  • Nianzhi JiaoEmail author
Progress

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.

Keywords

Prochlorococcus viruses Diversity Genomics Biogeochemical significance 

Notes

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).

References

  1. 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: e17722CrossRefGoogle Scholar
  2. Avrani S, Wurtzel O, Sharon I, Sorek R, Lindell D. 2011. Genomic island variability facilitates Prochlorococcus-virus coexistence. Nature, 474: 604–608CrossRefGoogle Scholar
  3. 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–E2200CrossRefGoogle Scholar
  4. 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: 2519–2529CrossRefGoogle Scholar
  5. 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: 1721–1731CrossRefGoogle Scholar
  6. Biller S J, Berube P M, Lindell D, Chisholm S W. 2015. Prochlorococcus: The structure and function of collective diversity. Nat Rev Microbiol, 13: 13–27CrossRefGoogle Scholar
  7. Breitbart M, Thompson L, Suttle C, Sullivan M. 2007. Exploring the vast diversity of marine viruses. Oceanography, 20: 135–139CrossRefGoogle Scholar
  8. Brum J R, Sullivan M B. 2015. Rising to the challenge: Accelerated pace of discovery transforms marine virology. Nat Rev Microbiol, 13: 147–159CrossRefGoogle Scholar
  9. 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: 167–192CrossRefGoogle Scholar
  10. 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: 340–343CrossRefGoogle Scholar
  11. 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: 442–448CrossRefGoogle Scholar
  12. 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: 1476–1491CrossRefGoogle Scholar
  13. 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: 1437–1455CrossRefGoogle Scholar
  14. 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: 619–628CrossRefGoogle Scholar
  15. 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: 9824–9829CrossRefGoogle Scholar
  16. 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: 1350–1357CrossRefGoogle Scholar
  17. Fuhrman J A. 1999. Marine viruses and their biogeochemical and ecological effects. Nature, 399: 541–548CrossRefGoogle Scholar
  18. 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: e2587CrossRefGoogle Scholar
  19. 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: 1492–1504CrossRefGoogle Scholar
  20. 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: 2283–2294CrossRefGoogle Scholar
  21. 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: 1732–1743CrossRefGoogle Scholar
  22. Hevroni G, Enav H, Rohwer F, Béjà O. 2015. Diversity of viral photosystem- I psaA genes. ISME J, 9: 1892–1898CrossRefGoogle Scholar
  23. Huang S, Zhang S, Jiao N, Chen F. 2015. Marine cyanophages demonstrate biogeographic patterns throughout the global ocean. Appl Environ Microbiol, 81: 441–452CrossRefGoogle Scholar
  24. Jiao N Z, Yang Y H. 2002. Ecological studies on Prochlorococcus in China seas. Chin Sci Bull, 47: 1243–1250CrossRefGoogle Scholar
  25. 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: 593–599CrossRefGoogle Scholar
  26. 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: 519–528CrossRefGoogle Scholar
  27. 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: 416–420CrossRefGoogle Scholar
  28. 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: 1997–2011CrossRefGoogle Scholar
  29. 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: 1827–1841CrossRefGoogle Scholar
  30. 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: 1856–1865CrossRefGoogle Scholar
  31. 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: 1356–1376CrossRefGoogle Scholar
  32. 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: 450–460CrossRefGoogle Scholar
  33. 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: 86–89CrossRefGoogle Scholar
  34. 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: 83–86CrossRefGoogle Scholar
  35. 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: 39–47CrossRefGoogle Scholar
  36. 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: 605–612CrossRefGoogle Scholar
  37. 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: 500–513CrossRefGoogle Scholar
  38. 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: 353–362CrossRefGoogle Scholar
  39. 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: 4530–4534CrossRefGoogle Scholar
  40. Partensky F, Hess W R, Vaulot D. 1999. Prochlorococcus, a marine photosynthetic prokaryote of global significance. Microbiol Mol Biol Rev, 63: 106–127Google Scholar
  41. Partensky F, Garczarek L. 2010. Prochlorococcus: Advantages and Limits of Minimalism. Annu Rev Mar Sci, 2: 305–331CrossRefGoogle Scholar
  42. 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: 320–336CrossRefGoogle Scholar
  43. Paul J H, Sullivan M B, Segall A M, Rohwer F. 2002. Marine phage genomics. Comp Biochem Physiol Part B-Biochem Mol Biol, 133: 463–476CrossRefGoogle Scholar
  44. 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: 1585–1589CrossRefGoogle Scholar
  45. Rohwer F, Edwards R. 2002. The phage proteomic tree: A genome-based taxonomy for phage. J Bacteriol, 184: 4529–4535CrossRefGoogle Scholar
  46. Rohwer F, Thurber R V. 2009. Viruses manipulate the marine environment. Nature, 459: 207–212CrossRefGoogle Scholar
  47. Sullivan M B, Waterbury J B, Chisholm S W. 2003. Erratum: Cyanophages infecting the oceanic cyanobacterium Prochlorococcus. Nature, 424: 1047–1051CrossRefGoogle Scholar
  48. 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: e144–806CrossRefGoogle Scholar
  49. 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: e234CrossRefGoogle Scholar
  50. 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: 2935–2951CrossRefGoogle Scholar
  51. 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: 2810–2823CrossRefGoogle Scholar
  52. 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: 3035–3056CrossRefGoogle Scholar
  53. Suttle C A. 2005. Viruses in the sea. Nature, 437: 356–361CrossRefGoogle Scholar
  54. Suttle C A. 2007. Marine viruses—Major players in the global ecosystem. Nat Rev Microbiol, 5: 801–812CrossRefGoogle Scholar
  55. 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–E764CrossRefGoogle Scholar
  56. 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: 1156–1164CrossRefGoogle Scholar
  57. 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: 3393–3399Google Scholar
  58. Wilhelm S W, Suttle C A. 1999. Viruses and nutrient cycles in the sea. Bioscience, 49: 781–788CrossRefGoogle Scholar
  59. 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: 109CrossRefGoogle Scholar
  60. Zeng Q, Chisholm S W. 2012. Marine viruses exploit their host’s twocomponent regulatory system in response to resource limitation. Curr Biol, 22: 124–128CrossRefGoogle Scholar
  61. Zhang R, Wei W, Cai L L. 2014. The fate and biogeochemical cycling of viral elements. Nat Rev Microbiol, 12: 850–851CrossRefGoogle Scholar
  62. 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: 15284CrossRefGoogle Scholar

Copyright information

© Science China Press and Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.State Key Laboratory of Marine Environmental Science, College of Ocean & Earth Sciences, Institute of Marine Microbes and EcospheresXiamen UniversityXiamenChina
  2. 2.Department of Ocean Science and Division of Life ScienceHong Kong University of Science and Technology, Clear Water BayHong KongChina

Personalised recommendations