Advertisement

Virologica Sinica

, Volume 30, Issue 4, pp 290–300 | Cite as

Genetic diversity and temporal dynamics of phytoplankton viruses in East Lake, China

  • Mei-Niang Wang
  • Xing-Yi Ge
  • Yong-Quan Wu
  • Xing-Lou Yang
  • Bing Tan
  • Yu-Ji Zhang
  • Zheng-Li Shi
Research Article

Abstract

Phytoplankton viruses are important components of aquatic ecosystems. However, their prevalence and genetic diversity in marine and freshwater systems are largely under estimated owing to the immense size of water bodies and limitations in virus discovery techniques. In this study, we conducted a 1-year survey of phytoplankton virus communities by collecting surface water monthly from an inland lake (East Lake) in China between May 2012 and April 2013. We examined four phytoplankton viruses, i.e., myoviruses, podoviruses, siphoviruses, and phycodnaviruses, and seven sets of primers were used to target conserved genes within these four species. In this year-long investigation, a total of 358 different virus-related sequences from four virus families were obtained. All virus families were detected in all months, except for cyanopodoviruses, which were only identified during eight of the 12 months surveyed. Moreover, virus abundance and diversity changed dynamically over time. Phylogenetic analysis revealed that the majority of viral sequences from East Lake, China displayed distinct clustering patterns compared with published sequences. These results supported the existence of a highly diverse and unique phytoplankton virus community in East Lake, China.

Keywords

cyanophage phycodnavirus genetic diversity dynamics East Lake 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Baudoux AC, Noordeloos AAM, Veldhuis MJW, Brussaard CPD. 2006. Virally induced mortality of Phaeocystis globosa during two spring blooms in temperate coastal waters. Aquat Microb Ecol, 44: 207–217.CrossRefGoogle Scholar
  2. Bergh O, Borsheim KY, Bratbak G, Heldal M. 1989. High Abundance of Viruses Found in Aquatic Environments. Nature, 340: 467–468.CrossRefPubMedGoogle Scholar
  3. Chen F, Suttle CA. 1995. Amplification of DNA-Polymerase Gene Fragments from Viruses Infecting Microalgae. Appl Environ Microbiol, 61: 1274–1278.PubMedCentralPubMedGoogle Scholar
  4. Chen F, Wang K, Huang SJ, Cai HY, Zhao MR, Jiao NZ, Wommack KE. 2009. Diverse and dynamic populations of cyanobacterial podoviruses in the Chesapeake Bay unveiled through DNA polymerase gene sequences. Environ Microbiol, 11: 2884–2892.CrossRefPubMedGoogle Scholar
  5. Clasen JL, Brigden SM, Payet JP, Suttle CA. 2008. Evidence that viral abundance across oceans and lakes is driven by different biological factors. Freshw Biol, 53: 1090–1100.CrossRefGoogle Scholar
  6. Clasen JL, Hanson CA, Ibrahim Y, Weihe C, Marston MF, Martiny JBH. 2013. Diversity and temporal dynamics of Southern California coastal marine cyanophage isolates. Aquat Microb Ecol, 69: 17–31.CrossRefGoogle Scholar
  7. Dunigan DD, Fitzgerald LA, Van Etten JL. 2006. Phycodnaviruses: A peek at genetic diversity. Virus Res, 117: 119–132.CrossRefPubMedGoogle Scholar
  8. Farnell-Jackson EA, Ward AK. 2003. Seasonal patterns of viruses, bacteria and dissolved organic carbon in a riverine wetland. Freshw Biol, 48:841–851.CrossRefGoogle Scholar
  9. Fitzgerald LA, Graves MV, Li X, Feldblyum T, Hartigan J, Van Etten JL. 2007. Sequence and annotation of the 314-kb MT325 and the 321-kb FR483 viruses that infect Chlorella Pbi. Virology, 358: 459–471.PubMedCentralCrossRefPubMedGoogle Scholar
  10. Fitzgerald LA, Wu PK, Gurnon JR, Biffinger JC, Ringeisen BR, Van Etten JL. 2010. Isolation of the phycodnavirus PBCV-1 by biological laser printing. J Virol Methods, 167: 223–225.CrossRefPubMedGoogle Scholar
  11. Fuhrman JA. 1999. Marine viruses and their biogeochemical and ecological effects. Nature, 399: 541–548.CrossRefPubMedGoogle Scholar
  12. Gao EB, Gui JF, Zhang QY. 2012. A Novel Cyanophage with a Cyanobacterial Nonbleaching Protein A Gene in the Genome. J Virol, 86: 236–245.PubMedCentralCrossRefPubMedGoogle Scholar
  13. Ge X, Wu Y, Wang M, Wang J, Wu L, Yang X, Zhang Y, Shi Z. 2013. Viral metagenomics analysis of planktonic viruses in East Lake, Wuhan, China. Virol Sin, 28: 280–290.CrossRefPubMedGoogle Scholar
  14. Gimenes MV, Zanotto PMD, Suttle CA, da Cunha HB, Mehnert DU. 2012. Phylodynamics and movement of Phycodnaviruses among aquatic environments. ISME J, 6: 237–247.PubMedCentralCrossRefPubMedGoogle Scholar
  15. Huang S, Wang K, Jiao N, Chen F. 2012. Genome sequences of siphoviruses infecting marine Synechococcus unveil a diverse cyanophage group and extensive phage-host genetic exchanges. Environ Microbiol, 14: 540–558.CrossRefPubMedGoogle Scholar
  16. Huang SJ, Wilhelm SW, Jiao NAZ, Chen F. 2010. Ubiquitous cyanobacterial podoviruses in the global oceans unveiled through viral DNA polymerase gene sequences. ISME J, 4: 1243–1251.CrossRefPubMedGoogle Scholar
  17. Jiang S, Steward G, Jellison R, Chu W, Choi S. 2004. Abundance, distribution, and diversity of viruses in alkaline, hypersaline Mono Lake, California. Microb Ecol, 47: 9–17.CrossRefPubMedGoogle Scholar
  18. Kumar S, Nei M, Dudley J, Tamura K. 2008. MEGA: A biologist-centric software for evolutionary analysis of DNA and protein sequences. Brief Bioinform, 9: 299–306.PubMedCentralCrossRefPubMedGoogle Scholar
  19. Labonte JM, Reid KE, Suttle CA. 2009. Phylogenetic Analysis Indicates Evolutionary Diversity and Environmental Segregation of Marine Podovirus DNA Polymerase Gene Sequences. Appl Environ Microbiol, 75: 3634–3640.PubMedCentralCrossRefPubMedGoogle Scholar
  20. Larsen JB, Larsen A, Bratbak G, Sandaa RA. 2008. Phylogenetic analysis of members of the Phycodnaviridae virus family, using amplified fragments of the major capsid protein gene. Appl Environ Microbiol, 74: 3048–3057.PubMedCentralCrossRefPubMedGoogle Scholar
  21. Liu YM, Yuan XP, Zhang QY. 2006. Spatial distribution and morphologic diversity of virioplankton in Lake Donghu, China. Acta Oecol, 29: 328–334.CrossRefGoogle Scholar
  22. Mann NH. 2003. Phages of the marine cyanobacterial picophytoplankton. Fems Microbiol Rev, 27: 17–34.CrossRefPubMedGoogle Scholar
  23. Nagasaki K, Tomaru Y, Nakanishi K, Hata N, Katanozaka N, Yamaguchi M. 2004. Dynamics of Heterocapsa circularisquama (Dinophyceae) and its viruses in Ago Bay, Japan. Aquat Microb Ecol, 34: 219–226.CrossRefGoogle Scholar
  24. Parvathi A, Zhong X, Jacquet S. 2012. Dynamics of various viral groups infecting autotrophic plankton in Lake Geneva. Adv Oceanogr Limnol, 3: 171–191(121).CrossRefGoogle Scholar
  25. Proctor LM, Fuhrman JA. 1990. Viral Mortality of Marine-Bacteria and Cyanobacteria. Nature, 343: 60–62.CrossRefGoogle Scholar
  26. Sabehi G, Shaulov L, Silver DH, Yanai I, Harel A, Lindell D. 2012. A novel lineage of myoviruses infecting cyanobacteria is widespread in the oceans. Proc Natl Acad Sci U S A, 109: 2037–2042.PubMedCentralCrossRefPubMedGoogle Scholar
  27. Schmidt HF, Sakowski EG, Williamson SJ, Polson SW, Wommack KE. 2014. Shotgun metagenomics indicates novel family A DNA polymerases predominate within marine virioplankton. ISME J, 8: 103–114.PubMedCentralCrossRefPubMedGoogle Scholar
  28. Short SM, Short CM. 2008. Diversity of algal viruses in various North American freshwater environments. Aquat Microb Ecol, 51: 13–21.CrossRefGoogle Scholar
  29. Sullivan MB, Coleman ML, Quinlivan V, Rosenkrantz JE, Defrancesco AS, Tan G, Fu R, Lee JA, Waterbury JB, Bielawski JP, Chisholm SW. 2008. Portal protein diversity and phage ecology. Environ Microbiol, 10: 2810–2823.PubMedCentralCrossRefPubMedGoogle Scholar
  30. Sullivan MB, Coleman ML, Weigele P, Rohwer F, Chisholm SW. 2005. Three Prochlorococcus cyanophage genomes: Signature features and ecological interpretations. Plos Biology, 3: 790–806.CrossRefGoogle Scholar
  31. Sullivan MB, Huang KH, Ignacio-Espinoza JC, Berlin AM, Kelly L, Weigele PR, De Francesco AS, Kern SE, Thompson LR, Young S, Yandava C, Fu R, Krastins B, Chase M, Sarracino D, Osburne MS, Henn MR, Chisholm SW. 2010. Genomic analysis of oceanic cyanobacterial myoviruses compared with T4-like myoviruses from diverse hosts and environments. Environ Microbiol, 12: 3035–3056.PubMedCentralCrossRefPubMedGoogle Scholar
  32. Sullivan MB, Krastins B, Hughes JL, Kelly L, Chase M, Sarracino D, Chisholm SW. 2009. The genome and structural proteome of an ocean siphovirus: a new window into the cyanobacterial 'mobilome'. Environ Microbiol, 11: 2935–2951.PubMedCentralCrossRefPubMedGoogle Scholar
  33. Suttle CA. 1994. The Significance of Viruses to Mortality in Aquatic Microbial Communities. Microb Ecol, 28: 237–243.CrossRefPubMedGoogle Scholar
  34. Suttle CA. 2000. In: Ecological, evolutionary, and geochemical consequences of viral infection of cyanobacteria and eukaryotic algae. Hurst CJ(ed), San Diego: Academic Press, pp. 247–296.Google Scholar
  35. Suttle CA. 2005. Viruses in the sea. Nature, 437: 356–361.CrossRefPubMedGoogle Scholar
  36. Suttle CA. 2007. Marine viruses - major players in the global ecosystem. Nat Rev Microbiol, 5: 801–812.CrossRefPubMedGoogle Scholar
  37. Thingstad TF. 2000. 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.CrossRefGoogle Scholar
  38. Thurber RV, Haynes M, Breitbart M, Wegley L, Rohwer F. 2009. Laboratory procedures to generate viral metagenomes. Nat Protoc, 4: 470–483.CrossRefPubMedGoogle Scholar
  39. Vrede K, Stensdotter U, Lindstrom ES. 2003. Viral and bacterioplankton dynamics in two lakes with different humic contents. Microb Ecol, 46: 406–415.CrossRefPubMedGoogle Scholar
  40. Wang GH, Murase J, Asakawa S, Kimura M. 2010. Unique viral capsid assembly protein gene (g20) of cyanophages in the floodwater of a Japanese paddy field. Biol Fert Soils, 46: 93–102.CrossRefGoogle Scholar
  41. Weinbauer MG, Christaki U, Nedoma A, Simek K. 2003. Comparing the effects of resource enrichment and grazing on viral production in a meso-eutrophic reservoir. Aquat Microb Ecol, 31: 137–144.CrossRefGoogle Scholar
  42. Wilhelm SW, Smith REH. 2000. Bacterial carbon production in Lake Erie is influenced by viruses and solar radiation. Can J Fish Aquat Sci, 57: 317–326.CrossRefGoogle Scholar
  43. Winter C, Bouvier T, Weinbauer MG, Thingstad TF. 2010. Trade- Offs between Competition and Defense Specialists among Unicellular Planktonic Organisms: the "Killing the Winner" Hypothesis Revisited. Microbiol Mol Biol Rev, 74: 42–57.PubMedCentralCrossRefPubMedGoogle Scholar
  44. Wommack KE, Colwell RR. 2000. Virioplankton: Viruses in aquatic ecosystems. Microbiology and Molecular Biology Rev, 64: 69–144.CrossRefGoogle Scholar
  45. Xia H, Wang M, Ge X, Wu Y, Yang X, Zhang Y, Li T, Shi Z. 2013. Study of the dynamics of Microcystis aeruginosa and its cyanophage in East Lake using quantitative PCR. Virol Sin, 28: 309–311.CrossRefPubMedGoogle Scholar
  46. Yoshida T, Nagasaki K, Takashima Y, Shirai Y, Tomaru Y, Takao Y, Sakamoto S, Hiroishi S, Ogata H. 2008. Ma-LMM01 infecting toxic Microcystis aeruginosa illuminates diverse cyanophage genome strategies. J Bacteriol, 190: 1762–1772.PubMedCentralCrossRefPubMedGoogle Scholar
  47. Zhang YZ, Adams B, Sun LW, Burbank DE, Van Etten JL. 2001. Intron conservation in the DNA polymerase gene encoded by Chlorella viruses. Virology, 285: 313–321.CrossRefPubMedGoogle Scholar
  48. Zheng CY, Wang GH, Liu JJ, Song CC, Gao HX, Liu XB. 2013. Characterization of the Major Capsid Genes (g23) of T4-Type Bacteriophages in the Wetlands of Northeast China. Microb Ecol, 65: 616–625.CrossRefPubMedGoogle Scholar
  49. Zhong X, Berdjeb L, Jacquet S. 2013. Temporal dynamics and structure of picocyanobacteria and cyanomyoviruses in two large and deep peri-alpine lakes. Fems Microbiol Ecol, 86: 312–326.CrossRefPubMedGoogle Scholar
  50. Zhong X, Jacquet S. 2013. Prevalence of Viral Photosynthetic and Capsid Protein Genes from Cyanophages in Two Large and Deep Perialpine Lakes. Appl Environ Microbiol, 79: 7169–7178.PubMedCentralCrossRefPubMedGoogle Scholar
  51. Zhong X, Jacquet S. 2014. Contrasting diversity of phycodnavirus signature genes in two large and deep western European lakes. Environ Microbiol, 16: 759–773.CrossRefPubMedGoogle Scholar
  52. Zhou Y, Lin J, Li N, Hu Z, Deng F. 2013. Characterization and genomic analysis of a plaque purified strain of cyanophage PP. Virol Sin, 28: 272–279.CrossRefPubMedGoogle Scholar

Copyright information

© Wuhan Institute of Virology, CAS and Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  • Mei-Niang Wang
    • 1
  • Xing-Yi Ge
    • 1
  • Yong-Quan Wu
    • 1
  • Xing-Lou Yang
    • 1
  • Bing Tan
    • 1
  • Yu-Ji Zhang
    • 1
  • Zheng-Li Shi
    • 1
  1. 1.Key Laboratory of Special Pathogens and Biosafety, Wuhan Institute of VirologyChinese Academy of SciencesWuhanChina

Personalised recommendations