Virioplankton as an important component of plankton in the Volga Reservoirs

  • A. I. Kopylov Papanin Institute for Biology of Inland Waters
  • E. A. Zabotkina Papanin Institute for Biology of Inland Waters
Keywords: viruses; viral lysis; heterotrophic bacteria; picocyanobacteria; microbial communities; freshwater ecosystems


The distribution of virioplankton, abundance and production, frequency of visibly infected cells of heterotrophic bacteria and autotrophic picocyanobacteria and their virus-induced mortality have been studied in mesotrophic and eutrophic reservoirs of the Upper and Middle Volga (Ivankovo, Uglich, Rybinsk, Gorky, Cheboksary, and Sheksna reservoirs). The abundance of planktonic viruses (VA) is on average by 4.6 ± 1.2 times greater than the abundance of bacterioplankton (BA). The distribution of VA in the Volga reservoirs was largely determined by the distribution of BA and heterotrophic bacterioplankton production (PB). There was a positive correlation between VA and BA and between VA and PB. In addition, BA and VA were both positively correlated with primary production of phytoplankton. Viral particles of 60 to 100 µm in size dominated in the phytoplankton composition. A large number of bacteria and picocyanobacteria with viruses attached to the surface of their cells were found in the reservoirs. Viruses as the most numerous component of plankton make a significant contribution to the formation of the planktonic microbial community biomass. The number of phages inside infected cells of bacteria and picocyanobacteria reached 74‒109 phages/cell. Easily digestible organic matter, which entered the aquatic environment as a result of viral lysis of bacteria and picocyanobacteria, could be an additional source of carbon for living bacteria. The results of long-term studies indicate a significant role of viruses in functioning of planktonic microbial communities in the Volga reservoirs.


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. Limnology and Oceanography, 52(6), 2519‒2529.

Bettarel, Y., Sime-Ngando, T., Bouvy, M., Arfi, R., & Amblard, C. (2005). Low consumption of virus-sized particles by heterotrophic nanoflagellates in two lakes of the French Massif Central. Aquatic Microbial Ecology, 39, 205‒209.

Binder, B. (1999). Reconsidering the relationship between virally induced bacterial mortality and frequency of infected cells. Aquatic Microbial Ecology, 18, 207‒215.

Bouvy, M., Bettarel, Y., Bouvier, C., Domaizon, I., Jacquet, S., Le Floc’h, E., Montanié, H., Mostajir, B., Sime-Ngando, T., Torréton, J. P., Vidussi, F., & Bouvier, T. (2011). Trophic interactions between viruses, bacteria and nanoflagellates under various nutrient conditions and simulated climate change. Environmental Microbiology, 13, 1842‒1857.

Bratbak, G., & Heldal, M. (2000). Viruses rule the waves – the smallest and most abundant members of marine ecosystems. Microbiology Today, 27, 171–173.

Bratbak, G., Thingstad, F., & Heldal, M. (1994). Viruses and the microbial loop. Microbial Ecology, 28, 209‒221.

Breitbart, M. (2012). Marine viruses: Truth or dare. Annual Review of Marine Science, 4, 425–448.

Clasen, J. L., Brigden, S. M., Payet, J. P., & Suttle, C. A. (2008). Evidence that viral abundance across oceans and lakes is driven by different biological factors. Freshwater Biology, 53(6), 1090‒1100.

Colombet, J., Charpin, M., Robin, A., Portelli, C., Amblard, C., Cauchie, H. M., & Sime-Ngando, T. (2009). Seasonal depth-related gradients in virioplankton: standing stock and relationships with microbial communities in Lake Pavin (France). Microbial Ecology, 58, 728–736.

Fischer, M. G., & Suttle, C. A. (2011). A virophage at the origin of large DNA transposons. Science, 332, 231‒234.

Fischer, U., & Velimirov, B. (2002). High control of bacterial production by viruses in a eutrophic oxbow lake. Aquatic Microbial Ecology, 27, 1‒12.

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

Gonzalez, J. M., & Suttle, C. A. (1993). Grazing by marine nanoflagellates on viruses and virus-sized particles: Ingestion and digestion. Marine Ecology Progress Series, 94(1), 1‒10.

Hanson, A. M., Berges, J. A., & Young, E. B. (2017). Viral morphological diversity and relationship to bacteria and chlorophyll across a freshwater trophic gradient in the Lake Michigan watershed. Hydrobiologia, 794, 93‒108.

Hardbower, D. M., Dolman, J. A., Glasner, D. R., Kendra, J. A., & Williamson, K. E. (2012). Optimization of viral profiling approaches reveals strong links between viral and bacterial communities in eutrophic freshwater lake. Aquatic Microbial Ecology, 67, 59‒76.

Hennes, K. P., & Simon, M. (1995). Significance of bacteriophages for controlling bacterioplankton growth in a mesotrophic lake. Applied and Environmental Microbiology, 61, 333‒340.

Hofer, J. S., & Sommaruga, R. (2001). Seasonal dynamics of viruses in an alpin lake: Importance of filamentous forms. Aquatic Microbial Ecology, 26, 1‒11.

Honjo, M., Matsui, K., Nakamura, R., Fuhrman, J. A., & Kawabata, Z. (2006). Diversity of virus-like agents killing Microcystis aeruginosa in a hyper-eutrophic pond. Journal of Plankton Research, 28, 407‒412.

Jiang, S. C., & Paul, J. H. (1998). Gene transfer by transduction in the marine environment. Applied and Environmental Microbiology, 64(8), 2780‒2787.

Jochem, F. (1988). On the distribution and importance of picocyanobacteria in a boreal inshore area (Kiel Bight, Western Baltic). Journal of Plankton Research, 10, 1009‒1022.

Keshri, J., Ram, A. S. P., Colombet, J., Perriere, P., Thouvenot, A., & Sime-Ngando, T. (2017). Differential impact of lytic viruses on the taxonomical resolution of freshwater bacterioplankton community structure. Water Research, 124, 129‒138.

Kopylov, A. I., Kosolapov, D. B., & Zabotkina, E. A. (2007). Viruses in the plankton of the Rybinsk reservoir. Microbiology, 76(6), 782‒790.

Kopylov, A. I., Kosolapov, D. B., & Zabotkina, E. A. (2011a). Impact of viruses on heterotrophic bacterioplankton and picocyanobacteria in reservoirs. Doklady Biological Sciences, 437(1), 91‒93.

Kopylov, A. I., Kosolapov, D. B., & Zabotkina, E. A. (2011b). Virus impact on heterotrophic bacterioplankton of water reservoirs. Microbiology, 80(2), 228‒236.

Kopylov, A. I., Kosolapov, D. B., Zabotkina, E. A., & Kosolapova, N. G. (2016). Trophic relationships between planktonic bacteria, heterotrophic nanoflagellates and viruses in a mesoeutrophic reservoir. Contemporary Problems of Ecology, 9(3), 297‒305.

Kopylov, A. I., Stroinov, Y. V., Zabotkina, E. A., Romanenko, A. V., & Maslennikova, T. S. (2013a). Heterotrophic microorganisms and viruses in the water of the Gorky reservoir during a period of anomalously high water temperature. Inland Water Biology, 6(2), 98‒105.

Kopylov, A. I., Stroinov, Y. V., Zabotkina, E. A., Romanenko, A. V., & Maslennikova, T. S. (2013b). Heterotrophic organisms and viruses in the Oka river and Cheboksary reservoir during the abnormally hot summer of 2010. Biology Bulletin, 40(3), 337‒341.

La Scola, D. C., Pagnier, I., Robert, C., & Barrassi, L. (2008). The virophage as a unique parasite of the giant mimivirus. Nature, 455, 100–104.

Landry, M. R., & Hassett, R. P. (1982). Estimating the grazing impact of marine micro-zooplankton. Marine Biology, 67, 283‒288.

Maclsaac, E. A., & Stockner, J. G. (1993). Enumeration of phototrophic picoplankton by autofluorescence microscopy. Handbook of methods in aquatic microbial ecology. Lewes Publishers, Boca Raton.

Mann, N. H. (2003). Phages of the marine cyanobacterial picophytoplankton. FEMS Microbiology Reviews, 27, 17–34.

Maranger, R., & Bird, D. F. (1995).Viral abundance in aquatic systems: A comparison between marine and fresh waters. Marine Ecology Progress Series, 121, 217‒226.

McDuff, R. E., & Chisholm, S. W. (1982). The calculation of in situ growth rates of phytoplankton populations from fractions of cells undergoing mitosis: A clarification. Limnology and Oceanography, 27, 783‒788.

Middelboe, M., Jacquet, S., & Weinbauer, M. G. (2008). Viruses in freshwater ecosystems: An introduction to the exploration of viruses in new aquatic habitats. Freshwater Biology, 53, 1069‒1075.

Noble, R. T., & Fuhrman, J. A. (1997). Viral decay and its causes in coastal waters. Applied and Environmental Microbiology, 63(1), 77‒83.

Noble, R. T., & Fuhrman, J. A. (1998). Use of SYBR Green for rapid epifluorescence count of marine viruses and bacteria. Aquatic Microbial Ecology, 14, 113‒118.

Noble, R. T., & Fuhrman, J. A. (1999). Breakdown and microbial uptake of marine viruses and other lysis products. Aquatic Microbial Ecology, 20, 1‒11.

Noble, R. T., & Steward, G. (2001). Estimating viral proliferation in aquatic samples. Methods in Microbiology, 30, 67‒84.

Norland, S. (1993). Section biomass. The relationship between biomass and volume of bacteria. In: Kemp, P., Sherr, B., Sherr, E., & Cole, J. (Eds.). Handbook of methods in aquatic microbial ecology. Lewis Publishers, Boca Raton.

Ortmann, A. C., Lawrence, J. E., & Suttle, C. A. (2002). Lysogeny and lytic viral production during a bloom of the cyanobacterium Synechococcus spp. Microbial Ecology, 43, 225‒231.

Peduzzi, P., & Schiemer, F. (2004). Bacteria and viruses in the water column of tropical freshwater reservoirs. Environmental Microbiology, 6(7), 707‒715.

Personnic, S., Domaizon, I., Sime-Ngando, T., & Jaquet, S. (2009). Seasonal variation of microbial abundances and virus-versus flagellate-induced mortality of picoplankton in three peri-alpine lakes. Journal of Plankton Research, 31(10), 1161‒1177.

Porter, K. G., & Feig, Y. S. (1980). The use DAPI for identifying and counting aquatic microflora. Limnology and Oceanography, 25(5), 943‒948.

Proctor, L. M., & Fuhrman, J. A. (1990). Viral mortality of marine bacteria and cyanobacteria. Nature, 343, 60‒62.

Ram, A. S. P., Boucher, D., Sime-Ngando, T., Debroas, D., & Romagoux, J. C. (2005). Phage bacteriolysis, protistan bacterivory potential, and bacterial production in a freshwater reservoir: Coupling with temperature. Microbial Ecology, 50, 64–72.

Ram, A. S. P., Colomber, J., Perriere, F., Thouvenot, A., & Sime-Ngando, T. (2015). Viral and grazer regulation of prokaryotic growth efficiency in temperate freshwater pelagic environments. FEMS Microbiology Ecology, 91(2), 1‒12.

Ram, A. S. P., Rasconi, S., Jobard, M., Palesse, S., Colombet, J., & Sime-Ngando, T. (2011). High lytic infection rates but low abundances of prokaryote viruses in a humic lake (Vassivière, Massit Central, France). Applied and Environmental Microbiology, 77(16), 5610‒5618.

Romanenko, V. I., & Kuznetsov, S. I. (1974). Ekologiya mikroorganizmov presnyh vodoyemov. Laboratornoe rukovodstvo [Ecology of microorganisms in fresh water bodies. Laboratory guidance]. Nauka, Leningrad (in Russian).

Simek, K., Pernthaler, J., Weinbauer, M. G., Hornák, K., Dolan, J. R., Nedoma, J., Masín, M., & Amann, R. (2001). Changes in bacterial community composition and dynamics and viral mortality rates associated with enhanced flagellate grazing in a mesoeutrophic reservoir. Applied and Environmental Microbiology, 67(6), 2723–2733.

Sime-Ngando, T. (2014). Environmental bicteriophges: Viruses of microbes in aquatic ecosystems. Frontiers in Microbiology, 5, 355.

Staniewski, M. A., & Short, S. M. (2014). Potential viral stimulation of primary production observed during experimental determinations of phytoplankton mortality. Aquatic Microbial Ecology, 71(3), 239–256.

Steward, G. F., Fandino, L. B., Hollibaugh, J. T., Whitledge, T. E., & Azam, F. (2007). Microbial biomass and viral infections of heterotrophic prokaryotes in the sub-surface layer of the Central Arctic Ocean. Deep-Sea Research I, 54, 1744‒1757.

Suttle, C. A. (2005). Viruses in the sea. Nature, 437, 356‒361.

Suttle, C. A. (2007). Marine viruses – major players in the global ecosystem. Nature Reviews Microbiology, 5(10), 801–812.

Suttle, C. A., & Chen, F. (1992). Mechanisms and rates of decay of marine viruses in seawater. Applied and Environmental Microbiology, 58(11), 3721‒3729.

Thomas, R., Berdjeb, L., Sime-Ngando, T., & Jaquet, S. (2011). Viral abundance, production, decay rates and life strategies (lysogeny versus lysis) in Lake Bourget (France). Environmental Microbiology, 13(3), 616–630.

Tijdens, M., Van de Waal, D. B., Slovakova, H., Hoogveld, H. L., & Gons, H. J. (2008). Estimates of bacterial and phytoplankton mortality caused by viral lysis and microzooplankton grazing in shallow eutrophic lake. Freshwater Biology, 53, 1126‒1144.

Vaqué, D., Boras, J., Torrent-Llagostera, F., Agustí, S., Arrieta, J. M., Lara, E., Castillo, Y. M., Duarte, C. M., & Sala, M. M. (2017).Viruses and protists induced-mortality of prokaryotes around the Antarctic Peninsula during the austral summer. Frontiers in Microbiology, 8, 241.

Vrede, K., Stensdotter, U., & Lindstrom, E. S. (2003). Viral and bacterioplankton dynamics in two lakes with different humic contents. Microbial Ecology, 46, 406–415.

Weinbauer, M. G. (2004). Ecology of prokaryotic viruses. FEMS Microbiology Reviews, 28(2), 127–181.

Weinbauer, M. G., & Hofle, M. G. (1998). Significance of virus lysis and flagellate grazing as factors controlling bacterioplankton production in a eutrophic lake. Applied and Environmental Microbiology, 64(2), 431‒438.

Weinbauer, M. G., & Rassoulzadegan, F. (2004). Are viruses driving microbial diversification and diversity? Environmental Microbiology, 5, 1‒11.

Wilhelm, S. W., & Matteson, A. R. (2008). Freshwater and marine virioplankton: A brief overview of commonalities and differences. Freshwater Biology, 53, 1076–1089.

Wilhelm, S. W., & Smith, R. E. N. (2000). Bacterial carbon production in Lake Erie is influenced by viruses and solar radiation. Canadian Journal of Fisheries and Aquatic Sciences, 57, 317–326.

Wommack, K. E., & Colwell, R. R. (2000). Virioplankton: Viruses in aquatic ecosystems. Microbiology and Molecular Biology Reviews, 64, 69‒114.

Yau, S., Lauro, F. M., Demaere, M. Z., Brown, M. V., Thomas, T., & Raftery, M. J. (2011). Virophage control of Antarctic algal host-virus dynamics. Proceedings of the National Academy of Sciences of the United States of America, 108(15), 6163–6168.

Zhang, Q.-Y., & Gui, J.-F. (2018). Diversity, evolutionary contribution and ecological roles of aquatic viruses. Science China, Life Sciences, 61(12), 1486‒1502.

Zheng, L., Liang, X., Shi, R., Li, P., Zhao, J., Li, G., Wang, S., Han, S., Radosevich, M., & Zhang, Y. (2020). Viral abundance and diversity of production fluids in oil reservoirs. Microorganisms, 8, 1429.

Zong, K. X., Suttle, C. A., Baudoux, A.-C., Derelle, E., Colombet, J., Cho, A., Caleta, J., Six, C., & Jacquet, S. (2018). A new freshwater ceanosiphovirus harboring integrase. Frontiers in Microbiology, 9, 2204.