Abstract—
Increasing interest in microbial communities of Arctic and Antarctic extreme environments, their taxonomic diversity, and forms and mechanisms of adaptation of inhabitants of Antarctic biotopes to extreme conditions determined the goal of the present work. Next generation sequencing of the 16S rRNA gene fragments was used to determine the taxonomic structure of microbial communities in soil samples from the Larsemann Hills and Bunger Hills. Revealed differences in the composition of predominant bacterial phyla and genera indicate that the type of the biotope developing on the soil surface and a combination of various physicochemical factors play a major role in formation of Antarctic microbial communities. High number of filterable forms of prokaryotes (FFP) was found in the communities. Analysis of the libraries of the 16S rRNA gene clones revealed that the FFP from three Larsemann Hills samples belonged to the phylum Proteobacteria. In all three samples, the dominant FFP group exhibited the highest similarity (99%) to an uncultured bacterial clone of the class Deltaproteobacteria revealed by assessment of bacterial diversity of rocks and groundwater of the Donghai County, China. The FFP capable of growth of standard nutrient media belonged to the phyla Actinobacteria, Bacteroidetes, Deinococcus-Thermus, Firmicutes, and Proteobacteria. Taking into account the data of high FFP number in the samples and their taxonomic composition, their significant contribution to stability of the bacterial composition of Antarctic soils may be suggested. The FFP fraction was mainly represented by bacterial dormant forms able to revert to active growth under favorable conditions. Rapid transition of a vegetative part of the population to small dormant forms under unfavorable conditions is probably one of the strategies enabling their survival in extreme environments. The FFP fraction also contained the cells belonging to novel bacterial species, probably ultramicrobacteria.
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REFERENCES
Abramov, A.A., Mironov, V.A., Lupachev, A.V., Fedorov-Davydov, D.G., Goryachkin, S.V., Mergelov, N.S., Ivashchenko, A.I., Lukin, V.V., and Gilichinskii, D.A., Geocryological conditions of polar oases, in Polyarnaya kriosfera i vosy sushi. Vklad Rossii v Mezhdunarodnyi polyarnyi god2007/2008 (Polar Cryosphere and Terrestrial Waters. Contribution of Russia to the Internationsl Polar Year 2007/2008), Kotlyakov, V.M., Ed., SPb.: Paulsen Editions, 2011, pp. 233–244.
Altschul, S.F., Gish, W., Miller, W., Myers, E.W., and Lipman, D.J., Basic local alignment search tool, J. Mol. Biol., 1990, vol. 215, pp. 403–410.
Barlow, R.S., Pemberton, J.M., Desmarchelier, P.M., and Gobius, K.S., Isolation and characterization of integron-containing bacteria without antibiotic selection, Antimicrob. Agents Chemother., 2004, vol. 48, pp. 838–842.
Caporaso, J.G., Kuczynski, J., Stombaugh, J., Bittinger, K., Bushman, F.D., Costello, E.K., Fierer, N., Peña, A.G., Goodrich, J.K., Gordon, J.I., Huttley, G.A., Kelley, S.T., Knights, D., Koenig, J.E., Ley, R.E., et al., QIIME allows analysis of high throughput community sequencing data, Nature Methods, 2010, vol. 7, pp. 335–336.
Chernov, T.I., Tkhakakhova, A.K., and Kutovaya, O.V., Assessment of diversity indices for the characterization of the soil prokaryotic community by metagenomic analysis, Euras. Soil Sci., 2015, vol. 48, pp. 410–415.
Cowan, D.A. Makhalanyane, T.P., Dennis, P.G., and Hopkins, D.W., Microbial ecology and biogeochemistry of continental Antarctic soils, Front. Microbiol., 2014, vol. 5, art. 154.
Duda, V.I., Suzina, N.E., Polivtseva, V.N., and Boronin, A.M., Ultramicrobacteria: formation of the concept and contribution of ultramicrobacteria to biology, Microbiology (Moscow), 2012, vol. 81, pp. 379–390.
Fomicheva, O.A., Polyanskaya, L.M., Zvyagintsev, D.G., Nikonov, V.V., Lukina, N.V., Orlova, M.A., and Isaeva, L.G., Population and biomass of soil microorganisms in old-growth primary spruce forests in the Northern Taiga, Euras. Soil Sci., 2006, vol. 39, pp. 1323–1331.
Golovchenko, A.V., Tikhonova, E.Yu., and Zvyagintsev, D.G., Abundance, biomass, structure, and activity of the microbial complexes of minerotrophic and ombrotrophic peatlands, Microbiology (Moscow), 2007, vol. 76, pp. 630–637.
Kryazhevskikh, N.A., Demkina, E.V., Loiko, N.G., Gal’chenko, V.F., El’-Registan, G.I., Baslerov, R.V., Kolganova, T.V., Soina, V.S., and Manucharova, N.A., Comparison of the adaptive potential of the Arthrobacter oxydans and Acinetobacter lwoffii isolates from permafrost sedimentary rock and the analogous collection strains, Microbiology (Moscow), 2013, vol. 82, pp. 29–42.
Kudinova, A.G., Lysak, L.V., Soina, V.S., Mergelov, N.S., Dolgikh, A.V., and Shorkunov, I.G., Bacterial communities in the soils of cryptogamic barrens of East Antarctica (the Larsemann Hills and Thala Hills oases), Euras. Soil Sci., 2015, vol. 48, pp. 276–287.
Lane, D.J., 16S/23S rRNA sequencing, in Nucleic Acid Techniques in Bacterial Systematics, Stackebrandt, E. and Goodfellow, M., Eds., N.Y.: Wiley, 1991, pp. 125–175.
Le, P.T., Makhalanyane, T.P., Guerrero, L.D., Vikram, S., Van de Peer, Y., and Cowan, D.A., Comparative metagenomic analysis reveals mechanisms for stress responsein hypoliths from extreme hyperarid deserts, Genome Biol. Evol., 2016, vol. 8, pp. 2737–2747.
Lysak, L.V., Skvortsova, I.N., and Dobrovol’skaya, T.G., Metody otsenki bakterial’nogo raznoobraziya pochv i identifikatsii pochvennykh bakterii (Methods for Assessment of Soil Bacterial Diversity and Identification of Soil Bacteria), Moscow: MAKS Press, 2003.
Maniatis, T., Fritsh, E.E., and Sambrook, J., Molecular Cloning. A Laboratory Manual, Cold Spring Harbor Laboratory, 1982.
Mergelov, N.S., Soils of wet valleys in the Larsemann Hills and Vestfold Hills oases (Princess Elizabeth Land, East Antarctica), Euras. Soil Sci., 2014, vol. 47, pp. 845–862.
Metody pochvennoi biokhimii i mikrobiologii (Methods of Soil Biochemistry and Microbiology), Zvyagintsev, G.G., Ed., Moscow: Mos. Gos. Univ., 1991.
Monchy, S., Benotmane, M.A., Janssen, P., Vallaeys, T., Taghavi, S., van der Lelie, D., and Mergeay, M., Plasmids pMOL28 and pMOL30 of Cupriavidus metallidurans are specialized in the maximal viable response to heavy metals, J. Bacteriol., 2007, vol. 189, pp. 7417–7425.
Pruesse, E., Quast, C., Knittel, K., Fuchs, B.M., Ludwig, W., Peplies, J., and Glöckner, F.O., SILVA: a comprehensive online resource for quality checked and aligned ribosomal RNA sequence data compatible with ARB, Nucleic Acids Res., 2007, vol. 35, pp. 7188–7196.
Sambrook, J., Edward, E.F., and Maniatis, T., Molecular Cloning: A Laboratory Manual, 2nd ed., N.Y.: Cold Spring Habour Laboratory, 1989.
Soina, V.S., Lysak, L.V., Konova, I.A., Lapygina, E.V., and Zvyagintsev, D.G., Study of ultramicrobacteria (Nanoforms) in soils and subsoil deposits by electron microscopy, Euras. Soil Sci., 2012, vol. 45, pp. 1048–1056.
Soina, V.S., Vorobiova, E.A., Zvyagintsev, D.G., and Gilichinsky, D.A., Preservation of cell structure in permafrost: a model for exobiology, Adv. Space Res., 1995, vol. 15, pp. 237–242.
Suzina, N.E., Esikova, T.Z., Oleinikov, R.R., Gafarov, B., Shorokhov, A.P., Polivtseva, V.N., Ross, D.V., Abashina, T.N., Duda, V.I., and Boronin, A.M., Comparative characteristics of free-living ultramicroscopical bacteria obtained from natural biotopes, Appl. Biochem. Microbiol.-, 2015, vol. 51, no. 2, pp. 159–168.
Takahashi, S., Tomita, J., Nishioka, K., Hisada, T., and Nishijima, M., Development of a prokaryotic universal primer for simultaneous analysis of bacteria and archaea using next-generation sequencing, PloS One, 2014, vol. 9, article e105592.
Vainshtein, M.B. and Kudryashova, E.B., About nannobacteria, Microbiology (Moscow), 2000, vol. 69, pp. 129–138.
Van Goethem, M.W., Makhalanyane, T.P., Valverde, A., Cary, S.C., and Cowan, D.A., Characterization of bacterial communities in lithobionts and soil niches from Victoria Valley, Antarctica, FEMS Microbiol. Ecol., 2016, vol. 92, article fiw051.
Wang, N.F., Zhang, T., Zhang, F., Wang, E.T., He, J.F., Ding, H., Zhang, B.T., Liu, J., Ran, X.B., and Zang, J.Y., Diversity and structure of soil bacterial communities in the Fildes Region (maritime Antarctica) as revealed by 454 pyrosequencing, Front. Microbiol., 2015, vol. 6, article 01188.
Zhang, E., Thibaut, L.M., Terauds, A., Raven, M., Tanaka, M.M., van Dorst, J., Wong, S.Y., Crane, S., and Ferrari, B.C., Lifting the veil on arid-to-hyperarid Antarctic soil microbiomes: a tale of two oases, Microbiome, 2020, vol. 8, pp. 1–12. Translated by E. Makeeva
ACKNOWLEDGMENTS
The authors of the article are deeply obliged to G.I. El-Registan, and V.A. Shcherbakova for their interest in the research and for valuable comments and corrections.
Funding
The work was supported by the Russian Foundation for Basic Research, project no. 18-34-00658. Samples were taken within the framework of State Order no. 0148-2019-0006 (Institute of Geography, Russian Academy of Sciences) with the logistical support of the Russian Antarctic Expedition.
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Kudinova, A.G., Petrova, M.A., Dolgikh, A.V. et al. Taxonomic Diversity of Bacteria and Their Filterable Forms in the Soils of Eastern Antarctica (Larsemann Hills and Bunger Hills). Microbiology 89, 574–584 (2020). https://doi.org/10.1134/S0026261720050136
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DOI: https://doi.org/10.1134/S0026261720050136