Abstract—
The research was aimed at detection of thermophilic microorganisms in Lake Baikal low-temperature sediments associated with discharge of gas-saturated fluids. Members of the order Clostridiales were revealed in enrichment cultures obtained from the bottom sediments at three sites (methane seep, oil-methane seep, and mud volcano). No thermophilic prokaryotes were found in the enrichment culture with sediment samples from a background area. The presence of thermophilic microorganisms at the sites of hydrocarbon discharge may result from their migration to the bottom surface with the gas-bearing mineralized fluid moving along the fracture zones. Unlike marine cold sediments, where the endospores of thermophilic bacteria belong to strict anaerobes existing due to fermentation of organic substrates or sulfate reduction, Lake Baikal sediments associated with discharge of gas-saturated fluids were found to contain facultatively anaerobic thermophilic prokaryotes.
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REFERENCES
Belkova, N.L., Parfenova, V.V., Suslova, M.Yu., Ahn, T.S., and Tazaki, K., Biodiversity and activity of the microbial community in the Kotelnikovsky hot springs (Lake Baikal), Biol. Bull. (Moscow), 2005, vol. 32, pp. 549–555.
Bonch-Osmolovskaya, E.A., Metabolic diversity of thermophilic prokaryotes–what’s new?, in Extremophiles: Microbiology and Biotechnology, Anitori, R., Ed., Beaverton: Horizon, 2012, pp. 109–130.
Chakraborty, A., Ellefson, E., Li, C., Gittins, D., Brooks, J.M., Bernard, B.B., and Hubert, C.R.J., Thermophilic endospores associated with migrated thermogenic hydrocarbons in deep Gulf of Mexico marine sediments, ISME J., 2018, vol. 12, pp. 1895–1906.
Chernitsyna, S.M., Mamaeva, E.V., Lomakina, A.V., Pogodaeva, T.V., Galach’yants, Yu.P., Bukin, S.V., Pimenov, N.V., Khlystov, O.M., and Zemskaya, T.I., Phylogenetic diversity of microbial communities of the Posolsk Bank bottom sediments, Lake Baikal, Microbiology (Moscow), 2016, vol. 85, pp. 672–680.
Cuylaerts, M., Naudts, L., Casier, R., Khabuev, A.V., Belousov, O.V., Kononov, E.E., Khlystov, O., and De Batist, M., Distribution and morphology of mud volcanoes and other fluid flow-related lake-bed structures in Lake Baikal, Russia, Geo-Mar. Lett., 2012, vol. 32, pp. 383–394.
De Rezende, J.R., Kjeldsen, K.U., Hubert, C.R.J., Finster, K., Loy, A., and Jørgensen, B.B., Dispersal of thermophilic Desulfotomaculum endospores into Baltic Sea sediments over thousands of years, ISME J., 2013, vol. 7, pp. 72–84.
Duchkov, A.D., Lysak, S.V., Golubev, V.A., Dorofeeva, R.P., and Sokolova, L.S., Heat flow and geotemperature fiald of the Baikal region, Geol. Geofiz., 1999, vol. 40, no. 3, pp. 287–303.
Fardeau, M.-L., Barsotti, V., Cayol, J.-L., Guasco, S., Michotey, V., Joseph, M., Bonin, P., and Ollivier, B., Caldinitratiruptor microaerophilus, gen. nov., sp. nov. isolated from a French hot spring (Chaudes-Aigues, Massif Central): a novel cultivated facultative microaerophilic anaerobic thermophile pertaining to the Symbiobacterium branch within the Firmicutes, Extremophiles, 2010, vol. 14, pp. 241–247.
Golubev, V.A., Heat flow through Lake Baikal depression, Doklady AN SSSR, 1979, vol. 245, no. 6, pp. 1333–1336.
Han, C., Gu, W., Zhang, X., Lapidus, A., Nolan, M., Copeland, A., Lucas, S., Del Rio, T.G., Tice, H., Cheng, J.F., Tapia, R., Goodwin, L., Pitluck, S., Pagani, I., Ivanova, N., et al., Complete genome sequence of Thermaerobacter marianensis type strain (7p75a), Stand. Genom. Sci., 2010, vol. 3, pp. 337–345.
Hubert, C., Arnosti, C., Brüchert, V., Loy, A., Vandieken, V., and Jørgensen, B.B., Thermophilic anaerobes in Arctic marine sediments induced to mineralize complex organic matter at high temperature, Environ. Microbiol., 2010, vol. 12, pp. 1089–1104.
Hubert, C., Loy, A., Nickel, M., Arnosti, C., Baranyi, C., Brüchert, V., Ferdelman, T., Finster, K., Christensen, F.M., De Rezende, J.R., Vandieken, V., and Jørgensen, B.B., A constant flux of diverse thermophilic bacteria into the cold Arctic seabed, Science, 2009, vol. 325, pp. 1541–1544.
Isaksen, M.F., Bak, F., and Jørgensen, B.B., Thermophilic sulfate-reducing bacteria in cold marine sediment, FEMS Microbiol. Ecol., 1994, vol. 14, pp. 1–8.
Kalashnikov, A.M., Gaisin, V.A., Sukhacheva, M.V., Namsaraev, B.B., Panteleeva, A.N., Nuyanzina-Boldareva, E.N., Kuznetsov, B.B., and Gorlenko, V.M., Anoxygenic phototrophic bacteria from microbial communities of Goryachinsk, Microbiology (Moscow), 2014, vol. 83, pp. 407–421.
Khlystov, O.M., De Batist, M., Shoji, H., Hachikubo, A., Nishio, S., and Naudt, L., Gas hydrate of Lake Baikal: discovery and varieties, J. Asian. Earth Sci., 2013, vol. 62, pp. 162–166.
Khlystov, O.M., Minami, H., Hachikubo, A., Yamashita, S., De Batist, M., Nauds, L., Khabuev, A.V., Chenskiy, A.G., Gubin, N.A., and Vorobyeva, S.S., Age of mud breccia from mud volcanoes in Academician Ridge, Lake Baikal, Geodyn. Tectonophys., 2017, vol. 8, pp. 923–932.
Klerkx, J., De Batist, M., Poort, J., Hus, R., VanRensbergen, P., Khlystov, O.M., and Granin, N., Tectonically controlled methane escape in Lake Baikal, in Advances in the Geological Storage of Carbon Dioxide, NATO Sci. Ser. IV. Earth Environ. Sci., 2006, vol. 65, pp. 203–219.
Kontorovich, A.E., Kashirtsev, V.A., Moskvin, V.I., Burshtein, L.M., Zemskaya, T.I., Kostyreva, E.A., Kalmychkov, G.V., and Khlystov, O.M., Petroleum potential of Baikal deposits, Russ. Geol. Geophys. (Novosibirsk), 2007, vol. 12, pp. 1046–1053.
Kovaleva, O.L., Merkel, A.Y., Novikov, A.A., Baslerov, R.V., Toshchakov, S.V., and Bonch-Osmolovskaya, E.A., Tepidisphaera mucosa gen. nov., sp. nov., a moderately thermophilic member of the class Phycisphaerae in the phylum Planctomycetes, and proposal of a new family, Tepidisphaeraceae fam. nov., and a new order, Tepidisphaerales ord. nov., Int. J. Syst. Evol. Microbiol., 2015, vol. 65, pp. 549–555.
Kozhov, M., Geography and hydrology of Baikal, in Lake Baikal and Its Life. Monographiae Biologicae, Dordrecht: Springer, 1963, vol. 11, pp. 5–55.
Kuzmin, M.I., Karabanov, E.B., Kawai, T., Williams, D., Bychinsky, V.A., Kerber, E.V., Kravchinsky, V., Bezrukova, E., Prokopenko, A.A., Geletii, V.F., Kalmychkov, G.V., Goreglyad, A.V., Antipin, V.S., Khomutova, M.Yu., Soshina, N.M., et al., Deep drilling on Lake Baikal: main results, Russ. Geol. Geophys. (Novosibirsk), 2001, vol. 42, pp. 8–34.
Lane, D.J., 16S/23S rRNA sequencing, in Nucleic Acid Techniques in Bacterial Systematics, Stackebrandt, E. and Goodfellow, M., Eds., New York: Wiley, 1991, pp. 115–175.
Lavrenteva, E.V., Shagzhina, A.P., Babasanova, O.B., Dunaevsky, Y.E., Barkhutova, D.D., and Namsaraev, Z.B., The study of two alkaliphilic thermophile bacteria of the Anoxybacillus genus, Appl. Biochem. Microbiolol., 2009, vol. 45, pp. 484–488.
Lebedeva, E.V., Of, S., Zumbragel, S., Kruse, M., Shagzhina, A., Lücker, S., Maixner, F., Lipski, A., Daims, H., and Spieck, E., Isolation and characterization of a moderately thermophilic nitrite-oxidizing bacterium from a geothermal spring, FEMS Microbiol. Ecol., 2010, vol. 75, pp. 195–204.
Müller, A.L., De Rezende, J.R., Hubert, C.R.J., Kjeldsen, K.U., Lagkouvardos, I., Berry, D., Jørgensen, B.B., and Loy, A., Endospores of thermophilic bacteria as tracers of microbial dispersal by ocean currents, ISME J., 2014, vol. 8, pp. 1153–1165.
Naudts, L., Khlystov, O., Granin, N., Chensky, A., Poort, J., and De Batist, M., Stratigraphic and structural control on the distribution of gas hydrates and active gas seeps on the Posolsky Bank, Lake Baikal, Geo-Mar. Lett., 2012, vol. 32, pp. 395–406.
Pavlova, O.N., Bukin, S.V., Gorshkov, A.G., Khanaeva, T.A., and Zemskaya, T.I., Microorganisms of Lake Baikal: from psychrophilic hydrocarbon-oxidizing aerobed to thermophilic mixotrophs, 1 Rossiiskii mikrobiologicheskii kongress (1st Russian Microbiological Congress), Reshetilova, T.A., Ed., Moscow: Voda: Khim. Ekol., 2017, pp. 68–69.
Pogodaeva, T.V., Lopatina, I.N., Khlystov, O.M., Egorov, A.V., and Zemskaya, T.I., Background composition of pore waters in Lake Baikal bottom sediments, J. Great Lakes Res., 2017, vol. 43, pp. 1030–1043.
Pogodaeva, T.V., Zemskaya, T.I., Golobokova, L.P., Khlystov, O.M., Minami, H., and Sakagami, H., Chemical composition of pore waters of bottom sediments in different Baikal basins, Russ. Geol. Geophys. (Novosibirsk), 2007, vol. 48, pp. 886–900.
Poort, J., Khlystov, O.M., Naudts, L., Duchkov, A.D., Shoji, H., Nishio, S., De Batist, M., Hachikubo, A., Kida, M., Minami, H., Manakov, A.Y., Kulikova, M.V., and Krylov, A.A., Thermal anomalies associated with shallow gas hydrates in the K-2 mud volcano, Lake Baikal, Geo-Mar. Lett., 2012, vol. 32, pp. 407–417.
Praktikum po mikrobiologii (Practical Course in Microbiology), Netrusov, A.I., Ed., Moscow: Akademiya, 2005.
Radnagueva, A.A., Lavrentieva, E.V., Budagaeva, V.G., Barkhutova, D.D., and Namsaraev, B.B., Organotrophic bacteria of the Baikal Rift Zone hot springs, Microbiology (Moscow), 2016, vol. 85, pp. 367–378.
Rozanov, A.S., Bryanskaya, A.V., Kotenko, A.V., and Peltek, S.E., Draft genome sequence of Thermoactinomyces sp. Gus2-1 isolated from the hot-spring Gusikha in Bargusin Valley (Baikal Rift Zone, Russia), Genomics Data, 2017, vol. 11, pp. 1–2. https://doi.org/10.1016/j.gdata.2016.11.014
Sambrook, J., Fritsch, E.F., and Maniatis, T., Molecular Cloning. A Laboratory Manual, New York: Cold Spring Harbor, 1989, vol. 2.
Sokolova, T.G., Kostrikina, N.A., Chernyh, N.A., Kolganova, T.V., Tourova, T.P., and Bonch-Osmolovskaya, E.A., Thermincola carboxydiphila gen. nov., sp. nov., a novel anaerobic, carboxydotrophic, hydrogenogenic bacterium from a hot spring of the Lake Baikal area, Int. J. Syst. Evol. Microbiol., 2005, vol. 55, pp. 2069–2073.
Spanevello, M.D. and Patel, B.K.C., Thermaerobacter, in Bergey’s Manual of Systematics of Archaea and Bacteria, Whitman, W.B., Ed., Wiley, 2015. https://doi.org/10.1002/9781118960608.gbm00730
Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M., and Kumar, S., MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods, Mol. Biol. Evol., 2011, vol. 28, pp. 2731–2739.
Van Rensbergen, P., De Batist, M., Klerkx, J., Hus, R., Poort, J., Vanneste, M., Granin, N., Khlystov, O., and Krinitsky, P., Sublacustrine mud volcanoes and methane seeps caused by dissociation of gas hydrates in Lake Baikal, Geology, 2002, vol. 30, pp. 631–634.
Verbolov, V.I., Currents and water exchange in Lake Baikal, Water Res., 1996, vol. 23, no. 4, pp. 381–391.
Volpi, M., Lomstein, B.A, Sichert, A., Roy, H., Jorgensen, B.B., and Kjeldsen, K.U., Identity, abundance, and reactivation kinetics of thermophilic fermentative endospores in cold marine sediment and seawater, Front. Microbiol., 2017, vol. 8, p. 131. https://doi.org/10.3389/fmicb.2017.00131
Yu, Z., Wu, C., Yang, G.Q., and Zhou, S.G., Planifilum caeni sp. nov., a novel member of Thermoactinomycete isolated from sludge compost, Curr. Microbiol., 2015, vol. 70, pp. 135–140.
Zhilina, T.N., Kevbrin, V.V., Tourova, T.P., Lysenko, A.M., Kostrikina, N.A., and Zavarzin, G.A., Clostridium alkalicellum sp. nov., an obligately alkaliphilic cellulolytic bacterium from a soda lake in the Baikal Region, Microbiology (Moscow), 2005, vol. 74, pp. 557–566.
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This work was carried out within the framework of the State Assignment no. 0345-2019-0007 (expedition studies) and 0345-2018-0001 (lithologic investigations and chemical analysis of pore waters) and was supported by the Russian Foundation for Basic Research, project no. 16-04-00181_а (microbiological and molecular biological studies).
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Pavlova, O.N., Lomakina, A.V., Novikova, A.S. et al. Thermophilic Bacteria in Lake Baikal Bottom Sediments Associated with Hydrocarbon Discharge. Microbiology 88, 335–342 (2019). https://doi.org/10.1134/S0026261719030081
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DOI: https://doi.org/10.1134/S0026261719030081