Abstract
This article presents the results of research into autochthonous bacteriophages, a previously unknown element in the structure of the microbial loop in the ecosystem of deep oligotrophic Lake Baikal. Transmission electron microscopy was used to study the morphological diversity of phages in the water column, surface microlayer, and benthic biofilms formed at the interface between water and geological rocks (marble, granite, mica, quartz, amphibolite, gabbro, and urtite). This article presents data on the dimensional structure of autochthonous bacteriophages, as well as their quantity, seasonal dynamics, and vertical distribution from the surface to the maximum depth (1200 m) when compared with the content of bacteria. Several morphotypes of Baikal autochthonous bacteriophages affecting Pseudomonas aeruginosa have been isolated and characterized by molecular-genetic methods. The complete genomes of giant phage PaBG from the Myoviridae family and phage MD8 from the Siphoviridae family have been determined.
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Ackermann, H.W., Frequency of morphological phage description in the year 2000, Arch. Virol., 2001, vol. 146, pp. 843–857.
Auguet, J. C., Montanie, H., and Lebaron, P., Structure of virioplankton in the Charente estuary (France): transmission electron microscopy versus pulsed field gel electrophoresis, Microb. Ecol., 2006, vol. 5, pp. 197–208.
Baikalovedenie (Baikal Studies), Sklyarov, E.V., Ed., Novosibirsk: Nauka, 2012, book 1.
Bergh, O., Borsheim, K.Y., Bratbak, G., and Heldal, M., High abundance of viruses found in aquatic environments, Nature, 1989, vol. 340, pp. 467–468.
Børsheim, K.Y., Bratbak, G., and Heldal, M., Enumeration and biomass estimation of planktonic bacteria and viruses by transmission electron microscopy, Appl. Environ. Microbiol., 1990, vol. 56, pp. 352–356.
Børsheim, K.Y., Native marine bacteriophages, FEMS Microbiol. Ecol., 1993, vol. 102, pp. 141–159.
Bratback, G., Heldal, M., Norland, S., and Thingstad, T.F., Viruses as partners in spring bloom microbial trophodynamics, Appl. Environ. Microbiol., 1990, vol. 56, no. 5, pp. 1400–1405.
Brum, J.R. and Sullivan, M.B., Rising to the challenge: accelerated pace of discovery transforms marine virology, Nat. Rev. Microbiol., 2015, vol. 13, pp. 147–159.
Brussaard, C.P.D., Marie, D., and Bratbak, G., Flow cytometric detection of viruses, J. Virol. Methods, 2000, vol. 85, nos. 1–2, pp. 175–182.
Butina, T.V., Belykh, O.I., Maksimenko, S.Y., and Belikov, S.I., Phylogenetic diversity of T4-like bacteriophages in Lake Baikal, East Siberia, FEMS Microbiol. Lett., 2010, vol. 309, no. 2, pp. 122–129.
Butina, T.V., Potapov, S.A., Belykh, O.I., and Belikov, S.I., Genetic diversity of cyanophages of the Myoviridae family as a constituentof the associated community of the Baikal sponge Lubomirskia baicalensis, Russ. J. Genet., 2015, vol. 51, no. 3, pp. 313–317.
Demuth, J., Neve, H., and Witzel, K., Direct electron microscopic study on the morphological diversity of bacteriophage populations in Lake Plußsee, Appl. Environ. Microbiol., 1993, vol. 59, no. 10, pp. 3378–3384.
Drucker, V.V. and Dutova, N.V., Phages of the Baikal Lake, Mezhdunarodnyi Baikal’skii mikrobiologicheskii simpozium “Mikroorganizmy v ekosistemakh ozer, rek i vodokhranilishch,” Tezisy dokladov (Int. Baikal Microbiological Symp. “Microorganisms in Ecosystems of Lakes, Rivers, and Reservoirs,” Abstracts of Papers), Irkutsk: Inst. Geogr., Sib. Otd., Ross. Akad. Nauk, 2003, p. 35.
Drucker, V.V. and Dutova, N.V., Study of the morphological diversity of bacteriophages in Lake Baikal, Dokl. Biol. Sci., 2006, vol. 410, no. 1, pp. 421–423.
Drucker, V.V. and Dutova, N.V., Bacteriophages as a new trophic link in the ecosystem of the deep-water Lake Baikal, Dokl. Biol. Sci., 2009, vol. 427, no. 1, pp. 339–342.
Drucker, V.V. and Maslennikov, A.A., Coli phages in Lake Baikal and their inflows, Materialy Vsesoyuznoi nauchnoi konferentsii “Sovremennye problemy ekologii, prirodopol’zovaniya i resursosberezheniya Pribaikal’ya” (Proc. All-Union Sci. Conf. “Modern Problems of Ecology, Nature Management, and Resource Saving in Baikal Region”), Irkutsk: Inst. Geogr., Sib. Otd., Ross. Akad. Nauk, 1998, p. 279.
Dutova, N.V. and Drucker, V.V., Viral community of bio-films forming on different substrates under natural conditions of Lake Baikal, Dokl. Biol. Sci., 2013, vol. 451, no. 1, pp. 238–240.
Fuhrman, J.A., Marine viruses and their biogeochemical and ecological effects, Nature, 1999, vol. 399, pp. 541–548.
Galachyants, A.D., Belkova, N.L., Sukhanova, E.V., Blinov, V.V., and Parfenova, V.V., Methods of neuston sampling for the quantitative characteristic of microbial communities of Lake Baikal, Inland Water Biol., 2016, vol. 9, no. 3, pp. 329–336.
Hendrix, R., Bacteriophage genomics, Curr. Opin. Microbiol., 2003, vol. 6, no. 5, pp. 506–511.
Hofer, J. and Sommaruga, R., Seasonal dynamics of viruses in an alpine lake: importance of filamentous forms, Aquat. Microb. Ecol., 2001, vol. 26, pp. 1–11.
Holmfeldt, K., Middelboe, M., Nybroe, O., and Riemann, L., Large variability in host strain susceptibility and phage host-range govern interactions between lytic marine phages and their flavobacterium hosts, Appl. Environ. Microbiol., 2007, vol. 73, no. 21, pp. 6730–6739.
Kopylov, A.I., The role of viruses in structure and functions of microbial communities in freshwater ecosystems, Zh. Sib. Fed. Univ., Biol., 2013, vol. 4, pp. 354–367.
Kopylov, A.I., Kosolapov, D.V., Zabotkina, E.A., and Kosolapova, N.G., Trophic relationships between planktonic bacteria, heterotrophic nanoflagellates and viruses in a mesoeutrophic reservoir, Contemp. Probl. Ecol., 2016a, vol. 9, no. 3, pp. 297–305.
Kopylov, A.I., Kosolapov, D.V., Zabotkina, E.A., and Rumyantseva, E.V., Viruses in bottom sediments of a mesotrophic reservoir (Rybinsk Reservoir, Upper Volga), Inland Water Biol., 2016b, vol. 9, no. 3, pp. 251–257.
Maniatis, T., Fritsch, E.F., and Sambrook, J. Molecular Cloning: A Laboratory Manual, Cold Spring Harbor, NY: Cold Spring Harbor Lab., 1982.
Mathias, C.B., Kirscher, A.K., and Vilimirov, B., Seasonal variations of virus abundance and viral control of the bacterial production in a backwater system of the Danube River, Appl. Environ. Microbiol., 1995, vol. 61, no. 10, pp. 3734–3740.
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, no. 2, pp. 113–118.
Noble, R.T. and Fuhrman, J.A., Breakdown and microbial uptake of marine viruses and other lysis products, Aquat. Microb. Ecol., 1999, vol. 20, pp. 1–11.
Parfenova, V.V., Gladkikh, A.S., and Belykh, O.I., Comparative analysis of biodiversity in the planktonic and biofilm bacterial communities in Lake Baikal, Microbiology (Moscow), 2013, vol. 82, no. 1, pp. 91–101.
Porter, K.G. and Feig, Y.S., The use of DAPI for identifying and counting aquatic microflora, Limnol. Oceanogr., 1980, vol. 25, pp. 943–948.
Potapov, S., Belykh, O., Krasnopeev, A., Gladkikh, A., Kabilov, M., Tupikin, A., and Butina, T., Assessing the diversity of the g23 gene of T4-like bacteriophages from Lake Baikal with high-throughput sequencing, FEMS Microbiol. Lett., 2017, vol. 364. doi https://doi.org/10.1093/femsle/fnx264
Proctor, L.M. and Fuhrman, J.A., Viral mortality of marine bacteria and cyanobacteria, Nature, 1990, vol. 343, pp. 60–62.
Sirotkin, A.K., Gavrilova, O.V., and Voloshko, L.N., Viruses in Lake Ladoga plankton, Dokl. Biol. Sci., 2001, vol. 378, nos. 1–6, pp. 254–257.
Sulcius, S., Staniulis, J., and Paskauskas, R., Morphology and distribution of phage-like particles in a eutrophic boreal lagoon, Oceanologia, 2011, vol. 53, no. 2, pp. 587–603.
Suttle, C.A., Viruses in the sea, Nature, 2005, vol. 437, pp. 356–361.
Suttle, C.A., Chan, A.M., and Cottrell, M.T., Infection of phytoplankton by viruses and reduction of primary productivity, Nature, 1990, vol. 347, pp. 467–469.
Sykilinda, N.N., Bondar, A.A., Gorshkova, A.S., Kurochkina, L.P., Kulikov, E.E., Shneider, M.M., Kadykov, V.A., Solovjeva, N.V., Kabilov, M.R., Mesyanzhinov, V.V., Vlassov, V.V., Drukker, V.V., and Miroshnikov, K.A., Complete genome sequence of the novel giant Pseudomonas phage PaBG, Genome Announce., 2014, vol. 2, no. 1, p. e00929–13.
Tapper, M.A. and Hicks, R.E., Temperate viruses and lysogeny in Lake Superior bacterioplankton, Limnol. Oceanogr., 1998, vol. 43, pp. 95–103.
Weinbauer, M.G., Ecology of prokaryotic viruses, FEMS Microbiol. Rev., 2004, vol. 28, pp. 127–181.
Weinbauer, M.G. and Peduzzi, P., Frequency, size and distribution of bacteriophages in different marine bacterial morphotypes, Mar. Ecol.: Progr. Ser., 1994, vol. 108, pp. 11–20.
Weitz, J.S. and Wilhelm, S.W., Ocean viruses and their effects on microbial communities and biogeochemical cycles, F1000 Biol. Rep., 2012, vol. 4, no. 17, pp. 1–8.
Wichels, A., Biel, S.S., Gelderblom, H.R., Brinkhoff, T., Muyzer, G., and Schutt, C., Bacteriophage diversity in the North Sea, Appl. Environ. Microbiol., 1998, vol. 64, no. 11, pp. 4128–4133.
Wilhelm, S.W. and Suttle, C.A., Viruses and nutrient cycles in the Sea, Bioscience, 1999, vol. 49, pp. 781–788.
Wommack, K.E. and Colwell, R.R., Virioplankton: viruses in aquatic ecosystems, Microbiol. Mol. Biol. Rev., 2000, vol. 64, no. 1, pp. 69–114.
Wommack, K.E., Hill, R.T., Kessel, M., Russek-Cohen, E., and Colwell, R.R., Distribution of viruses in the Chesapeake Bay, Appl. Environ. Microbiol., 1992, vol. 58, no. 9, pp. 2965–2970.
Zheng, Y.Z., Webb, R., Greenfield, P., and Reid, S., Improved method for counting virus and virus like particles, J. Virol. Methods, 1996, vol. 62, no. 2, pp. 153–159.
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Drucker, V.V., Belykh, O.I., Gorshkova, A.S. et al. Autochthonous Bacteriophages in the Microbial Loop Structure of Different Biotopes of Lake Baikal. Contemp. Probl. Ecol. 12, 143–154 (2019). https://doi.org/10.1134/S1995425519020045
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DOI: https://doi.org/10.1134/S1995425519020045