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Three-year survey of abundance, prevalence and genetic diversity of chlorovirus populations in a small urban lake

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Abstract

Inland water environments cover about 2.5 percent of our planet and harbor huge numbers of known and still unknown microorganisms. In this report, we examined water samples for the abundance, prevalence, and genetic diversity of a group of infectious viruses (chloroviruses) that infect symbiotic chlorella-like green algae. Samples were collected on a weekly basis for a period of 24 to 36 months from a recreational freshwater lake in Lincoln, Nebraska, and assayed for infectious viruses by plaque assay. The numbers of infectious virus particles were both host- and site-dependent. The consistent fluctuations in numbers of viruses suggest their impact as key factors in shaping microbial community structures in the water surface. Even in low-viral-abundance months, infectious chlorovirus populations were maintained, suggesting either that the viruses are very stable or that there is ongoing viral production in natural hosts.

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References

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

    Article  CAS  PubMed  Google Scholar 

  2. Mokili JL, Rohwer F, Dutilh BE (2012) Metagenomics and future perspectives in virus discovery. Curr Opin Virol 2:63–77

    Article  CAS  PubMed  Google Scholar 

  3. Bergh O, Borshelm KY, Bratbak G, Heldal M (1989) High abundance of viruses found in aquatic environments. Nature 340:467–468

    Article  CAS  PubMed  Google Scholar 

  4. Proctor LM, Fuhrman JA (1990) Viral mortality of marine bacteria and cyanobacteria. Nature 343:60–62

    Article  Google Scholar 

  5. Suttle CA (2005) Viruses in the sea. Nature 437:356–361

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  7. Bratbak G, Thingstad F, Heldal M (1994) Viruses and the microbial loop. Microb Ecol 28:209–221

    Article  CAS  PubMed  Google Scholar 

  8. Fuhrman JA (1999) Marine viruses and their biogeochemical and ecological effects. Nature 399:541–5488

    Article  CAS  PubMed  Google Scholar 

  9. Rohwer F, Thurber RV (2009) Viruses manipulate the marine environment. Nature 459:207–212

    Article  CAS  PubMed  Google Scholar 

  10. Maranger R, Bird DF (1995) Viral abundance in aquatic systems: a comparison between marine and fresh waters. Mar Ecol Prog Ser 121:217–226

    Article  Google Scholar 

  11. Weinbauer MG, Christaki U, Nedoma J, 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

    Article  Google Scholar 

  12. Matteson AR, Rowe JM, Ponsero AJ, Pimentel TM, Boyd PW, Wilhelm SW (2013) High abundances of cyanomyoviruses in marine ecosystems demonstrate ecological relevance. FEMS Microbiol Ecol 84:223–234

    Article  CAS  PubMed  Google Scholar 

  13. Short SM (2012) The ecology of viruses that infect eukaryotic algae. Environ Microbiol 14:2253–2271

    Article  PubMed  Google Scholar 

  14. Wilson WH, Van Etten JL, Allen MJ (2009) The Phycodnaviridae: the story of how tiny giants rule the world. In: Van Etten J (ed) Lesser known large dsDNA viruses. Current topics in microbiology and immunology, vol 328. Springer, Berlin, pp 1–42

    Chapter  Google Scholar 

  15. Wilson WH, Van Etten JL, Schroeder DC, Nagasaki K, Brussaard C, Bratbak G, Suttle C (2011) Phycodnaviridae. In: King AMQ, Adams MJ, Carstens EB, Lefkowitz EJ (eds) Virus taxonomy—ninth report, pp 249–262

  16. Van Etten JL, Van Etten CH, Johnson JK, Burbank DE (1985) A survey for viruses from fresh water that infect a eucaryotic chlorella-like green alga. Appl Environ Microbiol 49:1326–1328

    PubMed  PubMed Central  Google Scholar 

  17. Van Etten JL, Burbank DE, Schuster AM, Meints RH (1985) Lytic viruses infecting a chlorella like alga. Virology 140:135–143

    Article  PubMed  Google Scholar 

  18. Zhang YP, Burbank DE, Van Etten JL (1988) Chlorella viruses isolated in China. Appl Environ Microbiol 54:2170–2173

    CAS  PubMed  PubMed Central  Google Scholar 

  19. Yamada T, Higashiyama T, Fukuda T (1991) Screening of natural waters for viruses which infect chlorella cells. Appl Environ Microbiol 57:3433–3437

    CAS  PubMed  PubMed Central  Google Scholar 

  20. Yamada T, Shimomae A, Furukawa S, Takehara J (1993) Widespread distribution of chlorella viruses in Japan. Biosci Biotech Biochem 57:733–739

    Article  CAS  Google Scholar 

  21. Cho HH, Park HH, Kim JO, Choi TJ (2002) Isolation and characterization of chlorella viruses from freshwater sources in Korea. Mol Cells 14:168–176

    CAS  PubMed  Google Scholar 

  22. Van Etten JL, Dunigan DD (2012) Chloroviruses: not your everyday plant virus. Trends Plant Sci 17:1–8

    Article  PubMed  Google Scholar 

  23. Hoshina R, Iwataki M, Imamura N (2010) Chlorella variabilis and Micractinium reisseri sp. nov. Chlorellaceae, Trebouxiophyceae): Rediscription of the endosymbiotic green algae of Paramecium bursaria (Peniculia, Oligohymenophorea) in the 120th year. Phycol Res 58:188–201

    Article  CAS  Google Scholar 

  24. Proschold T, Darienko T, Silva PC, Reisser W, Krientz L (2011) The systematics of zoochlorella revisited employing an integrative approach. Environ Microbiol 13:350–364

    Article  CAS  PubMed  Google Scholar 

  25. EttenJL Van, Burbank DE, Kuczmarski D, Meints RH (1983) Virus infection of culturable chlorella-like algae and development of a plaque assay. Science 219:994–996

    Article  Google Scholar 

  26. Bubeck JA, Pfitzner AJ (2005) Isolation and characterization of a new type of chlorovirus that infects an endosymbiotic chlorella strain of the heliozoon Acanthocystis turfacea. J Gen Virol 86:2871–2877

    Article  CAS  PubMed  Google Scholar 

  27. Reisser W, Burbank DE, Meints SM, Meints RH, Becker B, Van Etten JL (1988) A comparison of viruses infecting two different chlorella-like green algae. Virology 167:143–149

    Article  CAS  PubMed  Google Scholar 

  28. Short SM, Short CM (2009) Quantitative PCR reveals transient and persistent algal viruses in Lake Ontario, Canada. Environ Microbiol 11:2639–2648

    Article  CAS  PubMed  Google Scholar 

  29. Short CM, Rusanova O, Short SM (2011) Quantification of virus genes provides evidence for seed-bank populations of phycodnaviruses in Lake Ontario, Canada. ISME J 5:810–821

    Article  CAS  PubMed  Google Scholar 

  30. Rozon RM, Short SM (2013) Complex seasonality observed amongst diverse phytoplankton viruses in the Bay of Quinte, an embayment of Lake Ontario. Freshw Biol 58:2648–2663

    Article  CAS  Google Scholar 

  31. Zhong X, Jacquet S (2014) Contrasting diversity of phycodnavirus signature genes in two large and deep western European lakes. Environ Microbiol 16:759–773

    Article  CAS  PubMed  Google Scholar 

  32. Wang MN, Ge XY, Wu YQ, Yang XL, Tan B, Zhang YJ, Shi ZL (2015) Genetic diversity and temporal dynamics of phytoplankton viruses in East Lake, China. Virol Sinica 30:290–300

    Article  Google Scholar 

  33. Yolken RH, Jones-Brando L, Dunigan DD, Kannan G, Dickerson F, Severance E, Sabunciyan S, Talbot CC, Prandovszky E, Gurnon JR, Agarkova IV, Leister F, Gressitt KL, Chen O, Deuber B, Ma F, Pletnikov MV, Van Etten JL (2014) Chlorovirus ATCV-1 is part of the human oropharyngeal virome and is associated with changes in cognitive functions in humans and mice. Proc Natl Acad Sci 111:16106–16111

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Van Etten JL, Burbank DE, Xia Y, Meints RH (1983) Growth cycle of a virus, PBCV-1, that infects chlorella-like algae. Virology 126:117–125

    Article  PubMed  Google Scholar 

  35. Kang JY, Goulder R, Woolston CJ (1993) Chlorella viruses in diverse fresh waters in North East England. Lett Appl Microb 16:214–216

    Article  Google Scholar 

  36. Kvitko K, Gromov BV (1984) New finding of a titratable infectious zoochlorella virus. Dokl Akad Nauk SSSR 279:998–999

    Google Scholar 

  37. Fitzgerald LA, Graves MV, Li X, Feldblyum T, Nierman WC, Van Etten JL (2007) Sequence and annotation of the 369-kb NY-2A and the 345-kb AR158 viruses that infect Chlorella NC64A. Virology 358:472–484

    Article  CAS  PubMed  Google Scholar 

  38. Jeanniard A, Dunigan DD, Gurnon JR, Agarkova IV, Kang M, Vitek J, Duncan G, McClung OW, Larsen M, Claverie JM, Van Etten JL, Blanc G (2013) Towards defining the chloroviruses: a genomic journey through a genus of large DNA viruses. BMC Genomics 14:158

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Van Etten JL, Schuster AM, Girton L, Burbank DE, Swinton D, Hattman S (1985) DNA methylation of viruses infecting a eukaryotic chlorella-like green alga. Nucleic Acids Res 13:3471–3478

    Article  PubMed  PubMed Central  Google Scholar 

  40. Van Etten JL, Schuster AM, Meints RH (1988) Viruses of eukaryotic chlorella-like algae. In: Koltin Y, Leibowitz MJ (eds) Viruses of fungi and simple eukaryotes. Marcel Dekker Inc, New York, pp 411–428

    Google Scholar 

  41. Yashchenko VV, Gavrilova OV, Rautian MS, Jakobsen KS (2012) Association of Paramecium bursaria chlorella viruses with Paramecium bursaria cells: ultrastructural studies. Eur J Protistol 48:149–159

    Article  PubMed  Google Scholar 

  42. Grasis JA, Lachnit T, Anton-Erxleben F, Lim YW, Schmieder R, Fraune S, Franzenburg S, Insua S, Machado G, Haynes M, Little M, Kimble R, Rosenstiel P, Rohwer FL, Bosch TC (2014) Species-specific viromes in the ancestral holobiont hydra. PloS One 9:e109952

    Article  PubMed  PubMed Central  Google Scholar 

  43. Cottrell MT, Suttle CA (1995) Dynamics of a lytic virus infecting the photosynthetic marine picoflagellate Micromonas pusilla. Limnol Oceanogr 40:730–739

    Article  Google Scholar 

  44. Furuta M, Schrader JO, Schrader HS, Kokjohn TA, Nyaga S, McCullough AK, Lloyd RS, Burbank DE, Landstein D, Lane L, Van Etten JL (1997) Chlorella virus PBCV-1 encodes a homolog of the bacteriophage T4 UV damage repair gene DenV. Appl Environ Microbiol 63:1551–1556

    CAS  PubMed  PubMed Central  Google Scholar 

  45. Dunigan DD, Cerny RL, Bauman AT, Roach JC, Lane LC, Agarkova IV, Wulser K, Yanai-Balser GM, Gurnon JR, Vitek JC, Kronschnabel BJ, Jeanniard A, Blanc G, Upton C, Duncan GA, McClung OW, Ma F, Van Etten JL (2012) Paramecium bursaria chlorella virus 1 proteome reveals novel architectural and regulatory features of a giant virus. J Virol 86:8821–8834

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Karakashian MW (1975) Symbiosis in Paramecium bursaria. Symp Soc Exp Biol 19:145–173

    Google Scholar 

  47. Meints RH, Lee K, Burbank DE, Van Etten JL (1984) Infection of a chlorella-like alga with the virus, PBCV-1: ultrastructure studies. Virology 138:341–346

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

Funding for this work was partially provided by the National Science Foundation-Experimental Program to Stimulate Competitive Research—Grant EPS-1004094 (JVE), Stanley Medical Research Institute—Grant 11R-0001 (JVE and DDD), and the Centers of Biomedical Research Excellence program of the National Center for Research Resources—Grant P20-RR15535 (JVE). OS and GW were supported by University of Nebraska Undergraduate Creative Activity and Research Experience and Agricultural Research Division scholarships. CM was supported by two summer fellowships from the Nebraska Center for Virology. We acknowledge Jim Gurnon for technical assistance. We thank Mike Archer at the Nebraska Department of Environmental Quality for providing the 2010 water analysis data.

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Authors and Affiliations

  1. Department of Plant Pathology, Plant Science Hall, University of Nebraska-Lincoln, Lincoln, NE, 68583, USA

    Cristian F. Quispe, Garrett Weber, David D. Dunigan & James L. Van Etten

  2. Nebraska Center for Virology, Morrison Center, University of Nebraska-Lincoln, Lincoln, NE, 68583, USA

    Cristian F. Quispe, Olivia Sonderman, Anya Seng, Brenna Rasmussen, Garrett Weber, Claire Mueller, David D. Dunigan & James L. Van Etten

  3. School of Biological Science, Manter Hall, University of Nebraska-Lincoln, Lincoln, NE, 68583, USA

    Cristian F. Quispe

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  1. Cristian F. Quispe
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Correspondence to Cristian F. Quispe.

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705_2016_2853_MOESM1_ESM.tif

Supplementary material 1 (TIFF 33070 kb) Supplementary Fig. S1 Plot representing the seasonal dynamics of chlorovirus populations over a 3-year period at site 1 and over a 2-year period at site 2 in Holmes Lake. Symbols represent the average values of plaque-forming units/ml (PFU/ml) for every week over each year. The x-axis indicates months, and the y-axis indicates PFU/ml of indigenous water. Each panel represents relative abundance for NC64A (A, B), Syngen (C, D) and SAG viruses (E, F) from each corresponding week and location

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Quispe, C.F., Sonderman, O., Seng, A. et al. Three-year survey of abundance, prevalence and genetic diversity of chlorovirus populations in a small urban lake. Arch Virol 161, 1839–1847 (2016). https://doi.org/10.1007/s00705-016-2853-4

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  • DOI: https://doi.org/10.1007/s00705-016-2853-4

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