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Anaerobic Methane Oxidation in Enrichment Cultures from Deep Sediments of a Mud Volcano Peschanka (South Baikal)

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Abstract

Under laboratory conditions, the microbial communities of bottom sediments of a mud volcano Peschanka (Lake Baikal) were found to carry out anaerobic methane oxidation (AOM). After 16 days of anaerobic cultivation of the enrichment cultures, methane content in the gas phase decreased, and microbial consortia were established. The content of carbon, nitrogen, and oxygen determined by energy dispersive X-ray spectroscopy (EDS) was higher than in the nearby sediment particles. The presence of bacteria of the NC10 phylum and archaea of the ANME-2d cluster was established by fluorescent in situ hybridization (FISH).

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References

  • Arshad, A., Speth, D.R., De Graaf, R.M., Op den Camp, H.J.M., Jetten, M.S., and Welte, C.U., A metagenomics- based metabolic model of nitrate-dependent anaerobic oxidation of methane by Methanoperedens-like archaea, Front. Microbiol., 2015, vol. 6, p. 1423.

    Article  PubMed  PubMed Central  Google Scholar 

  • Beal, E.J., House, C.H., and Orphan, V.J., Manganeseand iron-dependent marine methane oxidation, Science, 2009, vol. 325, pp. 184–187.

    Article  PubMed  CAS  Google Scholar 

  • Boetius, A., Ravenschlag, K., Schubert, C.J., Rickert, D., Widdel, F., Gieseke, A., Amann, R., Jørgensen, B.B., Witte, U., and Pfannkuche, O.A., Marine microbial consortium apparently mediating anaerobic oxidation of methane, Nature, 2000, vol. 407, pp. 623–626.

    Article  PubMed  CAS  Google Scholar 

  • Bol’shakov, A.M., and Egorov, A.V., On the application of phase equilibrium degassing fro gasometric research in water areas, Okeanologiya, 1987, vol. 37, no. 5, pp. 861–862.

    Google Scholar 

  • Chen, Y., Li, Yi.L., Zhou, G.-T., Li, H., Lin, Y.-T., Xiao, X., and Wang, F.-P., Biomineralization mediated by anaerobic methane-consuming cell consortia, Sci. Rep., 2014, vol. 4, p. 5696.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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, no. 6, pp. 672–680.

    Article  CAS  Google Scholar 

  • Ding, J., Ding, Z.W., Fu, L., Lu, Y.Z., Cheng, S.H., and Zeng, R.J., New primers for detecting and quantifying denitrifying anaerobic methane oxidation archaea in different ecological niches, Appl. Microbiol. Biotechnol., 2015, vol. 99, pp. 9805–9812.

    Article  PubMed  CAS  Google Scholar 

  • Egger, M., Rasigraf, O., Sapart, C.J., Jilbert, T., Jetten, M.S., Rockmann, T., van der Veen, C., Banda, N., Kartal, B., Ettwig, K., and Slomp, C., Iron-mediated anaerobic oxidation of methane in brackish coastal sediments, Environ. Sci. Technol., 2015, vol. 49, pp. 277–283.

    Article  PubMed  CAS  Google Scholar 

  • Ettwig, K.F., Butler, M.K., Le Paslier, D., Pelletier, E., Mangenot, S., Kuypers, M.M., Schreiber, F., Dutilh, B.E., Zedelius, J., de Beer, D., Gloerich, J., Wessels, H.J., van Alen, T., Luesken, F., Wu, M.L., et al., Nitrite-driven anaerobic methane oxidation by oxygenic bacteria, Nature, 2010, vol. 464, pp. 543–548.

    Article  PubMed  CAS  Google Scholar 

  • Ettwig, K.F., Shima, S., van de Pas-Schoonen, K.T., Kahnt, J., Medema, M.H., op den Camp, H.J.M., Jetten, M.S.M., and Strous, M., Denitrifying bacteria anaerobically oxidize methane in the absence of Archaea, Environ. Microbiol., 2008, vol. 10, pp. 3164–3173.

    Article  PubMed  CAS  Google Scholar 

  • Ettwig, K.F., Zhu, B., Speth, D., Keltjens, J.T., Jetten,M.S., and Kartal, B., Archaea catalyze iron-dependent anaerobic oxidation of methane, Proc. Natl. Acad. Sci. U. S. A., 2016, vol. 113, pp. 12792–12796.

    Article  CAS  Google Scholar 

  • Evans, P.N., Parks, D.H., Chadwick, G.L., Robbins, S.J., Orphan, V.J., Golding, S.D., and Tyson, G.W., Methane metabolism in the archaeal phylum Bathyarchaeota revealed by genome-centric metagenomics, Science, 2015, vol. 350, no. 6259, pp. 434–438.

    Article  PubMed  CAS  Google Scholar 

  • Glockner, F.O., Fuchs, B.M., and Amann, R., Bacterioplankton compositions of lakes and oceans: a first comparison based on fluorescence in situ hybridization, Appl. Environ. Microbiol., 1999, vol. 65, pp. 3721–3726.

    PubMed  PubMed Central  CAS  Google Scholar 

  • Haroon, M.F., Hu, S., Shi, Y., Imelfort, M., Keller, J., Hugenholtz, P., Yuan, Z., and Tyson, G.W., Anaerobic oxidation of methane coupled to nitrate reduction in a novel archaeal lineage, Nature, 2013, vol. 500, pp. 567–570.

    Article  PubMed  CAS  Google Scholar 

  • Hatzenpichler, R., Connon, S.A., Goudeau, D., Malmstrom, R.R., Woyke, T., and Orphan, V.J., Visualizing in situ translational activity for identifying and sorting slowgrowing archaeal−bacterial consortia, Proc. Natl. Acad. Sci. U. S. A., 2016, vol. 113, no. 28, pp. E4069–E4078.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • He, Z., Zhang, Q., Feng, Y., Luo, H., Pan, X., and Gadd, G.M., Microbiological and environmental significance of metal-dependent anaerobic oxidation of methane, Sci. Total Environ., 2018, vol. 610–611, pp. 759–768.

    Article  PubMed  CAS  Google Scholar 

  • Kadnikov, V.V., Mardanov, A., Beletsky, A.V., Shubenkova, O.V., Pogodaeva, T.N., Zemskaya, T.I., Ravin, N.V., and Skryabin, K.G., Microbial community structure in methane hydrate-bearing sediments of freshwater Lake Baikal, FEMS Microbiol. Ecol., 2012, vol. 79, pp. 348–358.

    Article  PubMed  CAS  Google Scholar 

  • Knittel, K., and Boetius, A., Anaerobic oxidation of methane: progress with an unknown process, Annul. Rev. Microbiol., 2009, vol. 63, pp. 311–334.

    Article  CAS  Google Scholar 

  • Knittel, K., Losekann, T., Boetius, A., Kort, R., and Amann, R., Diversity and distribution of methanotrophic archaea at cold seeps, Appl. Environ. Microbiol., 2005, vol. 71, pp. 467–479.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kuznetsov, S.I. and Dubinina, G.A., Metody izucheniya vodnykh mikroorganizmov (Methods of Investigation of Aquatic Microorganisms), Moscow: Nauka 1989.

    Google Scholar 

  • Lepland, A., Joosu, L., Kirsimäe, K., Prave, A.R., Romashkin, A.E., Crne, A.E., Martin, A.P., Fallick, A.E., Somelar, P., Üpraus, K., Mänd, K., Roberts, N.M.W., van Zuilen, M.A., Wirth, R., and Schreiber, A., Potential influence of sulphur bacteria on Palaeoproterozoic phosphogenesis, Nature Geosci., 2014, vol. 7, pp. 20–24.

    Article  CAS  Google Scholar 

  • Lomakina, A.V., Mamaeva, E.V., Galachyants, Y.P., Petrova, D.P., Pogodaeva, T.V., Shubenkova, O.V., Khabuev, A.V., Morozov, I.V., and Zemskaya, T.I., Diversity of Archaea in bottom sediments of the discharge area, Geomicrobiol. J., 2018, vol. 35, no. 1, pp. 50–63.

    Article  CAS  Google Scholar 

  • Lomakina, A.V., Pogodaeva, T.V., Morozov, I.V., and Zemskaya, T.I. Microbial communities of the discharge zone of oil- and gas-bearing fluids in low-mineral Lake Baikal, Microbiology (Moscow), 2014, vol. 83, no. 3, pp. 278–287.

    Article  CAS  Google Scholar 

  • Lu, Y.Z., Fu, L., Ding, J., Ding, Z.W., Li, N., and Zeng, R.J., Cr(VI) reduction coupled with anaerobic oxidation of methane in a laboratory reactor, Water Res., 2016, vol. 102, pp. 445–452.

    Article  PubMed  CAS  Google Scholar 

  • Neef, A., Amann, R., Schlesner, H., and Schlesner, K.-H., Monitoring a widespread bacterial group: in situ detection of planctomycetes with 16S rRNA-targeted probs, Microbiology (UK), 1998, vol. 144, pp. 3257–3266.

    Article  CAS  Google Scholar 

  • Norgi, K.A., Thamdrup, B., and Schubert, C.J., Anaerobic oxidation of methane in an iron-rich Danish freshwater lake sediment, Limnol. Oceanogr., 2013, vol. 58, pp. 546–554.

    Article  CAS  Google Scholar 

  • Och, L.M., Müller, B., Voegelin, A., Ulrich, A., Göttlicher, J., Steiniger, R., Mangold, S., Vologina, E.G., and Sturm, M., New insights into the formation and burial of Fe/Mn accumulations in Lake Baikal sediments, Chem. Geol., 2012, vols. 330–331, pp. 244–259.

    Article  CAS  Google Scholar 

  • Pernthaler, A., Dekas, A., Brown, T., Goffredi, S., Embaye, T., and Orphan, V., Diverse syntrophic partnerships from deep-sea methane vents revealed by direct cell capture and metagenomics, Proc. Natl. Acad. Sci. U. S. A., 2008, vol. 105, pp. 7052–7057.

    Article  PubMed  PubMed Central  Google Scholar 

  • Pimenov, N.V., Zakharova, E.E., Bryukhanov, A.L., Korneeva, V.A., Kuznetsov, B.B., Tourova, T.P., Pogodaeva, T.V., Kalmychkov, G.V., and Zemskaya, T.I., Activity and structure of the sulfate-reducing bacterial community in the sediments of the southern part of Lake Baikal, Microbiology (Moscow), 2014, vol. 83, nos. 1–2, pp. 47–55.

    Article  CAS  Google Scholar 

  • 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, no. 43, pp. 1030–1043.

    Article  CAS  Google Scholar 

  • Pol, L.W.H., de Castro Lopes, S.I., Lettinga, G., and Lens, P.N.L., Anaerobic sludge granulation, Water Res., 2004, vol. 38, pp. 1376–1389.

    Article  CAS  Google Scholar 

  • Raghoebarsing, A.A., Pol, A., van de Pas-Schoonen, K.T., Smolders, A.J., Ettwig, K.F., Rijpstra, W.I., Schouten, S., Damsté, J.S., Op den Camp, H.J., Jetten, M.S., and Strous, M., A microbial consortium couples anaerobic methane oxidation to denitrification, Nature, 2006, vol. 440, pp. 918–921.

    Article  PubMed  CAS  Google Scholar 

  • Reeburgh, W.S., Methane consumption in Cariaco Trench waters and sediments, Earth Planet. Sc. Lett., 1976, vol. 28, pp. 337–344.

    Article  CAS  Google Scholar 

  • Riedinger, N., Formolo, M.J., Lyons, T.W., Henkel, S., Beck, A., and Kasten, S., An inorganic geochemical argument for coupled anaerobic oxidation of methane and iron reduction in marine sediments, Geobiology, 2014, vol. 12, pp. 172–181.

    Article  PubMed  CAS  Google Scholar 

  • Schreiber, L., Holler, T., Knittel, K., Meyerdierks, A., and Amann, R., Identification of the dominant sulfate-reducing bacterial partner of anaerobic methanotrophs of the ANME-2 clade, Environ. Microbiol., 2010, vol. 12, pp. 2327–2340.

    PubMed  CAS  Google Scholar 

  • Sivan, O., Adler, M., Pearson, A., Gelman, F., Bar-Or, I., John, S.G., and Eckert, W., Geochemical evidence for iron-mediated anaerobic oxidation of methane, Limnol. Oceanogr., 2011, vol. 56, pp. 1536–1544.

    Article  CAS  Google Scholar 

  • Timmers, P.H., Welte, C.U., Koehorst, J.J., Plugge, C.M., Jetten, M.S., and Stams, A.J., Reverse methanogenesis and respiration in methanotrophic archaea, Archaea, 2017, vol. 2017, p. 1654237.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Torres, N.T., Och, L.M., Hauser, P.C., Furrer, G., Brandl, H., Vologina, E., Sturm, M., Bürgmann, H., and Müller, B., Early diagenetic processes generate iron and manganese oxide layers in the sediments of Lake Baikal, Siberia, Environ. Sci.: Proc. Imp., 2014, vol. 16, pp. 879–889.

    CAS  Google Scholar 

  • Vanwonterghem, I., Evans, P.N., Parks, D.H., Jensen, P.D., Woodcroft, B.J., Hugenholtz, P., and Tyson, G.W., Methylotrophic methanogenesis discovered in the archaeal phylum Verstraetearchaeota, Nat. Microbiol., 2016, vol. 1, article ID 16170.

  • Vigneron, A., Cruaud, P., Pignet, P., Caprais, J.-C., Gayet, N., Cambon-Bonavita, M.-A., Godfroy, A., and Toffin, L., Bacterial communities and syntrophic associations involved in anaerobic oxidation of methane process of the Sonora Margin cold seeps, Guaymas Basin, Environ. Microbiol., 2014, vol. 16, pp. 2777–2790.

    Article  PubMed  CAS  Google Scholar 

  • Weber, H.S., Habicht, K.S., and Thamdrup, B., Anaerobic methanotrophic archaea of the ANME-2d cluster are active in a low-sulfate, iron-rich freshwater sediment, Front. Microbiol., 2017, vol. 8, p. 619.

    PubMed  PubMed Central  Google Scholar 

  • Weber, H.S., Thamdrup, B., and Habicht, K.S., High sulfur isotope fractionation associated with anaerobic oxidation of methane in a lowsulfate, iron-rich environment, Front. Earth Sci., 2016, vol. 4, p. 61.

    Article  Google Scholar 

  • Welte, C.U., Rasigraf, O., Vaksmaa, A., Versantvoort, W., Arshad, A., Op den Camp, H.J., Jetten, M.S., Lüke, C., and Reimann, J., Nitrate- and nitrite-dependent anaerobic oxidation of methane, Environ. Microbiol. Rep., 2016, vol. 8, pp. 941–955.

    Article  PubMed  CAS  Google Scholar 

  • Zemskaya, T.I., Khlystov, O.M., Egorov, A.V., Pogodaeva, T.V., Kalmychkov, G.V., Shubenkova, O.V., Chernitsyna, S.M., Vorob’eva, S.S., and Grachev, M.A., Integrated studies of gas hydrate manifestations in the sediments of Lake Baikal mud volcanoes, in Protsessy v biosfere: izmemeniya pochvenno-rastitel’nogo pokrova i territorial’nykh vod RF, krugovorot veshchestv pod vliyaniem global’nykh izmenenii klimata i katastroficheskikh protsessov (Processes in the Boisphere: Changes in Soil and Plant Cover and RF Territorial Waters, Matter Turnover Caused by Global Climatic Changes and Catastrophic Processes), Zavarzin, G.A. and Kudeyarov, V.N., Eds., Pushchino-Moscow, 2008, vol. 4, pp. 125–152.

    Google Scholar 

  • Zemskaya, T.I., Lomakina, A.V., Mamaeva, E.V., Zakharenko, A.S., Pogodaeva, T.V., Petrova, D.P., and Galachyants, Yu.P., Bacterial communities in sediments of Lake Baikal from areas with oil and gas discharge, Aquat. Microb. Ecol., 2015, vol. 76, pp. 95–109.

    Article  Google Scholar 

  • Zemskaya, T.I., Pogodaeva, T.V., Shubenkova, O.V., Chernitsina, S.M., Dagurova, O.P., Buryukhaev, S.P., Namsaraev, B.B., Khlystov, O.M., Egorov, A.V., Krylov, A.A., and Kalmychkov, G.V., Geochemical and microbiological characteristics of sediments near the Malenky mud volcano (Lake Baikal, Russia), with evidence of Archaea intermediate between the marine anaerobic methanotrophs ANME-2 and ANME-3, Geo-Mar. Lett., 2010, vol. 30, nos. 3–4, pp. 411–425.

    CAS  Google Scholar 

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Correspondence to A. V. Lomakina.

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Original Russian Text © A.V. Lomakina, E.V. Mamaeva, T.V. Pogodaeva, G.V. Kalmychkov, I.A. Khal’zov, T.I. Zemskaya, 2018, published in Mikrobiologiya, 2018, Vol. 87, No. 3.

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Lomakina, A.V., Mamaeva, E.V., Pogodaeva, T.V. et al. Anaerobic Methane Oxidation in Enrichment Cultures from Deep Sediments of a Mud Volcano Peschanka (South Baikal). Microbiology 87, 317–325 (2018). https://doi.org/10.1134/S0026261718030049

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