Abstract
Interactions of the main components of microbial planktonic food web (bacteria, heterotrophic nanoflagellates, and viruses) were studied in a protected overgrown littoral zone of the Rybinsk Reservoir (Upper Volga). The effect of colonial bird settlements (the Laridae family) on these processes was determined. The following systems exhibited significant negative correlations: “heterotrophic nanoflagellates–large rod-shaped bacteria” (“predator–prey”), “viruses-bacteriophages–bacterial products” (“parasite–host”) and “heterotrophic nanoflagellates–viruses-bacteriophages”. Relations between biotic factors controlling bacterial development were more pronounced outside the zone affected by colonial bird settlements. Near the bird colony the role of viruses in mortality of planktonic bacteria increased. Reproduction of bacterial cells accelerated in response to the increase in feeding activity of heterotrophic nanoflagellates. Virusesbacteriophages and heterotrophic nanoflagellates probably eliminate different targets until medium-sized cells become predominant in the bacterial community. Then heterotrophic nanoflagellates consume bacterial cells infected with viruses.
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Andersson, A., Larsson, U., and Hagström, A., Size-selective grazing by a microflagellate on pelagic bacteria, Mar. Ecol. Prog. Ser., 1986, vol. 33, pp. 51–57.
Auguet, J.C., Montanié, H., Hartmann, H.J., Lebaron, P., Casamayor, E.O., Catala, P., and Delmas, D., Potential effect of freshwater virus on the structure and activity of bacterial communities in the Marennes-Oleron bay (France), Microb. Ecol., 2009, vol. 57, pp. 295–306.
Berdjeb, L., Pollet, T., Domaizon, I., and Jacquet S., Effect of grazers and viruses on bacterial community structure and production in two contrasting trophic lakes, BMC Microbiol., 2011, vol. 11, pp. 88–100.
Bettarel, Y., Sime-Ngando, T., Bouvy, M., Arfi, R., and Amblard, C., Low consumption of virus-sized particles by heterotrophyc nanoflagellates in two lakes of the French Massif Central, Aquat. Microb. Ecol., 2005, vol. 39, pp. 205–209.
Caron, D.A., Technique for enumeration of heterotrophic and phototrophic nanoplankton, using epifluorescence microscopy and comparison with other procedures, Appl. Environ. Microbiol., 1983, vol. 46, pp. 491–498.
Colombet, J. and Sime-Ngando, T., Seasonal depthrelated gradients in virioplankton: lytic activity and comparison with protistan grazing potential in lake Pavin (France), Microb. Ecol., 2012, vol. 64, pp. 67–78.
del Giorgio, P.A., Gasol, J.M., Vaque, D., Mura, P., Agusti, S., and Duarte, C.M., Bacterioplankton community structure: protists control net production and the proportion of active bacteria in a coastal marine community, Limnol. Oceanogr., 1996, vol. 41, no. 6, pp. 1169–1179.
Fischer, U.R. and Velimirov, B., High control of bacteria production by viruses in a eutrophic oxbow lake, Aquat. Microb. Ecol., 2002, vol. 27, vol. 1, pp. 1–12.
Fukuda, M., Matsuyama, J., Katano, T., Nakano, S., and Dazzo, F., Assessing primary and bacterial production rates in biofilms on pebbles in Ishite Stream, Japan, Microb. Ecol., 2006, vol. 52, pp. 1–9.
Gonzalez, J.M. and Suttle, C.A., Grazing by marine nanoflagellates on viruses and viral-sized particles ingestion and digestion, Mar. Ecol. Prog. Ser., 1993, vol. 94, pp. 1–10.
Jacquet, S., Domaizon, I., Personnic, S., and Sime-Ngando, T. Do small grazers influence virus-induced mortality of bacteria in Lake Bourget (France)?, Fund. Appl. Limnol. Arch. Hydrobiol., 2007, vol. 170, pp. 125–132.
Jurgens, K., Predation on bacteria and bacterial resistance mechanisms: comparative aspects among different predator groups in aquatic systems, Microbiology Monographs, Berlin: Springer-Verlag, 2007, vol. 4, pp. 57–92.
Kopylov, A.I. and Kosolapov, D.B., Bakterioplankton vodokhranilishch Verkhnei i Srednei Volgi (Bacterioplankton of the Upper and Mid-Volga Reservoirs), Moscow, 2008.
Kopylov, A.I., Kosolapov, D.B., and Zabotkina, E.A., Viruses in the plankton of the Rybinsk Reservoir, Microbiology (Moscow), 2007, vol. 76, no. 6, pp. 782–790.
Martiny, J.B., Riemann, L., Marston, M.F., and Middelboe, M., Antagonistic coevolution of 433 marine planktonic viruses and their hosts, Ann. Rev. Mar. Sci., 2014, vol. 6, pp. 393–414.
Miki, T. and Jacquet, S., Complex interactions in the microbial world: underexplored key links between viruses, bacteria and protozoan grazers in aquatic environments, Aquat. Microb. Ecol., 2008, vol. 51, pp. 195–208.
Newell, S.Y. and Christian, R.R., Frequency of dividing cells as an estimator of bacterial productivity, Appl. Environ. Microbiol., 1981, vol. 42, pp. 23–31.
Noble, R.T. and Fuhrman, J.A., Use of SYBR Green I for rapid epifluorescence counts of marine viruses and bacteria, Aquat. Microb. Ecol., 1998, vol. 14, pp. 113–118.
Norland, S., The relationships between biomass and volume of bacteria, in Handbook of Methods in Aquatic Microbial Ecology, Kemp, P., Sherr, B., Sherr, E., and Cole, J., Eds., Boca Raton: Lewis, 1993, pp. 303–308.
Porter, K.G. and Feig, Y.S., The use of DAPI for identifying and counting of aquatic microflora, Limnol. Oceanogr., 1980, vol. 25, pp. 943–948.
Riemann, B. and Søndergaard, M., Measurements of diel rates of bacterial secondary production in aquatic environments, Appl. Environ. Microbiol., 1984, vol. 47, pp. 632–638.
Rohwer, F. and Thurber, R.V., Viruses manipulate the marine environment, Nature, 2009, vol. 459, no. 7244, pp. 207–212.
Romanenko, V.I., Mikrobiologicheskie protsessy produktsii i destruktsii organicheskogo veshchestva vo vnutrennikh vodoemakh (Microbiological Processes of Production and Destruction of Organic Matter in Internal Water Bodies), Leningrad: Nauka, 1985.
Rumyantseva, E.V., Kosolapov, D.B., Kosolapova, N.G., and Kulakov, D.V., Dynamics of planktic microorganisms and viruses in the littoral zone of the Rybinsk reservoir: influence of water-bird colonies, Inland Water Biol., 2013, vol. 6, no. 4, pp. 276–284.
Rumyantseva, E.V., Kosolapov, D.B., Kosolapova, N.G., and Levanova, Y.V., Bacterioplankton in the area of gull colonies (Laridae) in the Rybinsk Reservoir, Inland Water Biol., 2015, vol. 8, no. 2, pp. 136–146.
Rumyantseva, E.V., Sakharova, E.G., Kosolapov, D.B., Kosolapova, N.G., Meteleva, N.Yu., and Korneva, L.G., Bacterio-and phytoplankton of protected littoral of a hightrophicity plain Reservoir: effect of colonial birds, Voda: Khim. Ekol., 2014, no. 1 (66), pp. 64–70.
Tanaka, T., Fujita, N., and Taniguchi, A., Predator-prey eddy in heterotrophic nanoflagellate-bacteria relationships in a coastal marine environment: a new scheme for predator-prey associations, Aquat. Microb. Ecol., 1997, vol. 13, pp. 249–256.
Thingstad, T.F., Element of a theory for the mechanisms controlling abundance, diversity, and biogeochemical role of lytic bacterial viruses in aquatic system, Limnol. Oceanogr., 2000, vol. 45, pp. 1320–1328.
Torreton, J.-E. and Dufour, E., Bacterioplankton production determined by DNA synthesis, protein synthesis, and frequency of dividing cells in Tuamotu Atoll lagoons and surrounding ocean, Microb. Ecol., 1996, vol. 32, pp. 185–202.
Tuomi, P., Bacterial carbon production in the northern Baltic: a comparison of thymidine incorporation and FDC based methods, Mar. Ecol. Prog. Ser., 1997, vol. 153, pp. 59–66.
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Original Russian Text © E.V. Rumyantseva, N.G. Kosolapova, D.B. Kosolapov, 2016, published in Mikrobiologiya, 2016, Vol. 85, No. 5, pp. 588–597.
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Rumyantseva, E.V., Kosolapova, N.G. & Kosolapov, D.B. Relations between bacterioplankton, heterotrophic nanoflagellates, and virioplankton in the littoral zone of a large plain reservoir: Impact of bird colonies. Microbiology 85, 620–628 (2016). https://doi.org/10.1134/S0026261716050143
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DOI: https://doi.org/10.1134/S0026261716050143