Skip to main content
Log in

Halophilic-psychrotrophic bacteria of an Alaskan cryopeg—a model for astrobiology

  • Published:
Paleontological Journal Aims and scope Submit manuscript

Abstract

Cryopegs, lenses of hypersaline unfrozen soil or water within permafrost, are a model for astrobiology, since free water can only be present on cryogenic bodies and planets in the form of brine. In this paper the diversity of aerobic halophilic-psychrotrophic microorganisms from an Alaskan cryopeg (Barrow Cape) were studied and described for the first time. This cryopeg is characterized by a constant subzero temperature (–7°C), high salinity (total mineralization is about 120 g/L) and isolation from external influences for a geologically significant period of time. Our study has revealed a large number of microorganisms capable of growth at low temperature (4°C) in a wide range of salinities from 5 to 250 g/L of NaCl, the latter being 3 times higher than the natural salt concentration of the Alaskan cryopeg. The microorganisms identified are comprised of four major phyla: Actinobacteria (genera Brevibacterium, Citricoccus, Microbacterium), Firmicutes (genus Paenibacillus), Bacteroidetes (genus Sphingobacterium), and Proteobacteria (genus Ochrobactrum).

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Backermans, C., Tsapin, A.I., Souza-Egipsy, V., Gilichinsky, D.A., and Nealson, K.H., Reproduction and metabolism at–10°C of bacteria isolated from Siberian permafrost, Environ. Microbiol., 2003, vol. 5, no. 4, pp. 321–326.

    Article  Google Scholar 

  • Baulin, V.V., Ivanova, N.V., Rivkin, F.M., Chernyad’ev, V.P., and Shamanova, I.I., Coastal cryolithozone northwestern Yamal: Problems of development, Kriosf. Zem., 2005, vol. 9, no. 1, pp. 28–37.

    Google Scholar 

  • Black, R., Gubik Formation of Quaternary Age in northern Alaska, US Geol. Survey Prof. Paper 302-C, Washington, DC: United States Gov. Print. Off., 1964, pp. 59–91.

    Google Scholar 

  • Colangelo-Lillis, J., Eicken, H., Carpenter, S.D., and Deming, J.W., Evidence for marine origin and microbial–viral habitability of sub-zero hypersaline aqueous inclusions within permafrost near Barrow, Alaska, FEMS Microbiol. Ecol., 2016, vol. 92, no. 5. http://dx.doi.org/ fiw053. doi 10.1093/femsec/fiw053

    Google Scholar 

  • Demidov, N.E., Gilichinsky, D.A., Mironov, V.A., and Shmakova, L.A., Cryosphere of the Earth and a search for life on Mars, Kriosf. Zem., 2012, vol. 16, no. 4, pp. 67–82.

    Google Scholar 

  • Ewert, M., Carpenter, S.D., Colangelo-Lillis, J., and Deming, J.W., Bacterial and extracellular polysaccharide content of brine-wetted snow over Arctic winter first-year sea ice, J. Geophys. Res. Oce., 2013, vol. 118, no. 2, pp. 726–735.

    Article  Google Scholar 

  • Felsenstein, J., Confidence limits on phylogenies: An approach using the bootstrap, Evolution, 1985, vol. 39, no. 4, pp. 783–791.

    Article  Google Scholar 

  • Fotiev, S.M., Hydrochemical method for estimation of the paleotemperature of rocks on the Arctic coast, Kriosf. Zem., 1997, vol. 1, no. 2, pp. 29–35.

    Google Scholar 

  • Fotiev, S.M., Kriogennyi metamorfizm porod i podzemnykh vod (Cryogenic Meamorphism of Rocks and Underground Waters), Moscow: Akad. Izd–vo GEO, 2009.

    Google Scholar 

  • Geokriologiya SSSR. Evropeiskaya territoriya SSSR (Geocryology of the USSR: European Territory of the USSR), Ershov, E.D., Eds., Moscow: Nedra, 1988.

  • Geokriologiya SSSR. Zapadnaya Sibir’ (Geocryology of the USSR: Western Siberia), Ershov, E.D, Eds., Moscow: Nedra, 1989.

  • Gilichinsky, D.A., Permafrost model of extraterrestrial habitat, in Astrobiology, Horneck, G. and Baumstark-Khan, C., Eds., Berlin: Springer, 2002, pp. 125–142.

    Chapter  Google Scholar 

  • Gilichinsky, M., Demidov, N., and Rivkina, E., Morphometry of volcanic cones on Mars in perspective of astrobiological research, Int. J. Astrobiol., 2015, vol. 14, no. 4, pp. 537–545.

    Article  Google Scholar 

  • Gilichinsky, D.A., Rivkina, E.M., Shcherbakova, V.A., Laurinavichyus, K.S., Komarov, I.A., and Volkov, N.G., Cryopegs and their inhabitants—a model for astrobiology, Kriosf. Zem., 2003a, vol. 7, no. 3, pp. 73–84.

    Google Scholar 

  • Gilichinsky, D., Rivkina, E., Shcherbakova, V., Laurinavichuis, K., and Tiedje, J., Supercooled water brines within permafrost— an unknown ecological niche for microorganisms: Amodel for astrobiology, Astrobiology, 2003b, vol. 3, no. 2, pp. 331–341.

    Article  Google Scholar 

  • Gilichinsky, D., Rivkina, E., Bakermans, C., Shcherbakova, V., Petrovskaya, L., Ozerskaya, S., Ivanushkina, N., Kochkina, G., Laurinavichuis, K., Pecheritsina, S., Fattakhova, R., and Tiedje, J.M., Biodiversity of cryopegs in permafrost, FEMS Microbiol. Ecol., 2005, vol. 53, no. 1, pp. 117–128.

    Article  Google Scholar 

  • Guan, T.W., Zhao, K., Xiao, J., Liu, Y., Xia, Z.F., Zhang, X.P., and Zhang, L.L., Brevibacterium salitolerans sp. nov., an actinobacterium isolated from salt-lake sediment, Int. J. Syst. Evol. Microbiol., 2010, vol. 60, no. 12, pp. 2991–299.

    Article  Google Scholar 

  • Jiang, S., Chen, M., Su, S., Yang, M., Li, A., Zhang, C., Lin, M., Zhang, W., and Luo, X., Sphingobacterium arenae sp. nov., isolated from sandy soil, Int. J. Syst. Evol. Microbiol., 2014, vol. 64, no. 1, pp. 248–253.

    Article  Google Scholar 

  • Jukes, T.H. and Cantor, C.R., Evolution of protein molecules, in Mammalian Protein Metabolism, Munro, H.N., Ed., New York: Academic, 1969, pp. 121–132.

    Google Scholar 

  • Kochkina, G.A., Ivanushkina, N.E., Akimov, V.N., Gilichinsky, D.A., and Ozerskaya, S.M., Halopsychrotolerant fungi of the genus Geomyces from cryopegs and marine deposits of the Arctic Region, Mikrobiologiya, 2007, vol. 76, no. 1, pp. 39–48.

    Google Scholar 

  • Mancinelli, R.L., Fahlen, T.F., Landheim, R., and Klovstad, M.R., Brines and evaporites: Analogs for martian life, Adv. Space Res., 2004, vol. 33, pp. 1244–1246.

    Article  Google Scholar 

  • Mancinelli, R.L., Microbial life in brines, evaporites and saline sediments: The search for life on Mars, Adv. Astrobiol. Biogeophys, 2005, vol. 4, pp. 277–297.

    Google Scholar 

  • Matsui, T., Kato K., Namihira, T., Shinzato, N., and Semba, H., Stereospecific degradation of phenylsuccinate by actinomycetes, Chemosphere, 2009, vol. 76, no. 9, pp. 1278–1282.

    Article  Google Scholar 

  • Metody obshchei Bakteriologii (Methods of General Bacteriology), Gerkhardt, F. et al., Eds., Moscow: Mir, 1983, vol. 3.

  • Neizvestnov, Ya.V. and Semenov, Yu.P., Underground cryopegs of the shelf and islands of the Soviet Arctic, Trudy II Mezhdunarodnoi konferentsii po merzlotovedeniyu: Doklady i soobshcheniya (Proceedings of the 2nd International Conference on Geocryology), Yakutsk, 1973, vol. 5, pp. 98–103.

    Google Scholar 

  • Nelson, D.M., Glawe, A.J., Labeda, D.P., Cann, I.K., and Mackie, R.I., Paenibacillus tundrae sp. nov. and Paenibacillus xylanexedens sp. nov., psychrotolerant, xylan-degrading bacteria from Alaskan tundra, Int. J. Syst. Evol. Microbiol., 2009, vol. 59, no. 7, pp. 1708–1714.

    Article  Google Scholar 

  • Niederberger, T.D., Perreault, N.N., Tille, S., Lollar, B.S., Lacrampe-Couloume, G., Andersen, D., Greer, C.W., Pollard, W., and Whyte, L.G., Microbial characterization of a subzero, hypersaline methane seep in the Canadian High Arctic, ISME J., 2010, vol. 4, no. 10, pp. 1326–1339.

    Article  Google Scholar 

  • Nielsen, M.B., Kjeldsen, K.U., and Ingvorsen, K., Description of Citricoccus nitrophenolicus sp. nov., a paranitrophenol degrading actinobacterium isolated from a wastewater treatment plant and emended description of the genus Citricoccus Altenburger et al. 2002, Antonie van Leeuwenhoek, 2011, vol. 99, no. 3, pp. 489–499.

    Article  Google Scholar 

  • Novototskaya-Vlasova, K., Petrovskaya, L., Kryukova, E., Rivkina, E., Dolgikh, D., and Kirpichnikov, M., Expression and chaperone-assisted refolding of a new cold-active lipase from Psychrobacter cryohalolentis K5(T), Protein Expr. Purif., 2013, vol. 91, no. 1, pp. 96–103.

    Article  Google Scholar 

  • Novototskaya-Vlasova, K., Petrovskaya, L., Yakimov, S., and Gilichinsky, D., Cloning, purification, and characterization of a cold-adapted esterase produced by Psychrobacter cryohalolentis K5T from Siberian cryopeg, FEMS Microbiol. Ecol., 2012, vol. 82, no. 2, pp. 367–375.

    Article  Google Scholar 

  • Ozerskaya, S.M., Ivanushkina, N.E., Kochkina, G.A., Fattakhova, R.N., and Gilichinsky, D.A., Mycelial fungi in cryopegs, Int. J. Astrobiol., 2004, vol. 3, no. 4, pp. 327–331.

    Article  Google Scholar 

  • Park, H.J. and Kim, D., Isolation and characterization of humic substances-degrading bacteria from the subarctic Alaska grasslands, J. Basic Microbiol., 2015, vol. 55, no. 1, pp. 54–61.

    Article  Google Scholar 

  • Pecheritsyna, S.A., Rivkina, E.M., Akimov, V.N., and Shcherbakova, V.A., Desulfovibrio arcticus sp. nov., a psychrotolerant sulfatereducing bacterium from a cryopeg, Int. J. Syst. Evol. Microbiol., 2012, vol. 62, pp. 33–37.

    Article  Google Scholar 

  • Pecheritsyna, S.A., Shcherbakova, V.A., Kholodov, A.L., Akimov, V.N., Abashina, T.N., Suzina, N.E., and Rivkina, E.M., Microbiological analysis of cryopegs of the Varandeiskii Peninsula on the coast of the Barent Sea, Mikrobiologiya, 2007, vol. 76, pp. 694–701.

    Google Scholar 

  • Petrovskaya, L.E., Novototskaya-Vlasova, K.A., Spirina, E.V., et al., Lipolytic enzymes of microorganisms from cryopegs of permafrost, Dokl. Akad. Nauk, 2012, vol. 445, no. 1, pp. 102–105.

    Google Scholar 

  • Ponomarev, V.M., Podzemnye vody territorii s moshchnoi tolshchei mnogoletnemerzlykh gornykh porod (Underground Waters of the Territory with Thick Strata of Perineal Permafrost Rocks), Ponomarev, V.M., Ed., Moscow: Akad. Nauk SSSR, 1960.

    Google Scholar 

  • Rivkina, E., Laurinavichius, K., McGrath, J., Tiedje, J.M., Shcherbakova, V., and Gilichinsky, D., Microbial life in permafrost, Adv. Space Res., 2004, vol. 33, pp. 1215–1221.

    Article  Google Scholar 

  • Rivkina, E., Shcherbakova, V., Laurinavichius, K., Petrovskaya, L., Krivushin, K., Kraev, G., Pecheritsina, S., and Gilichinsky, D., Biogeochemistry of methane and methanogenic archaea in permafrost, FEMS Microbiol. Ecol., 2007, vol. 61, no. 1, pp. 1–15.

    Article  Google Scholar 

  • Saitou, N. and Nei, M., The neighbor-joining method: A new method for reconstructing phylogenetic trees, Mol. Biol. Evol., 1987, vol. 4, no. 4, pp. 406–425.

    Google Scholar 

  • Schumann, P., Rainey, F.A., Burghardt, J., Stackebrandt, E., and Weiss, N., Reclassification of Brevibacterium oxydans (Chatelain and Second 1966) as Microbacterium oxydans comb. nov, Int. J. Syst. Bacteriol., 1999, vol. 49, no. 1, pp. 175–177.

    Article  Google Scholar 

  • Shcherbakova, V., Chuvilskaya, N., Rivkina, E., Demidov, N., Uchaeva, V., Suetin, S., Suzina, N., and Gilichinsky, D., Celerinatantimonas yamalensis sp. nov., a cold-adapted diazotrophic bacterium from a cold permafrost brine, Int. J. Syst. Evol. Microbiol., 2013, vol. 63, pp. 4421–4427.

    Article  Google Scholar 

  • Shcherbakova, V., Chuvil’skaya, N., Rivkina, E., Laurinavichus, K., Suetin, S., Pecheritsina, S., Lysenko, A., and Gilichinsky, D., New halotolerant bacterium from a cryopeg in permafrost: Description of Psychrobacter muriicola sp. nov., Mikrobiologiya, 2009, vol. 78, no. 1, pp. 98–105.

    Google Scholar 

  • Shcherbakova, V.A., Chuvilskaya, N.A., Rivkina, E.M., Pecheritsyna, S.A., Laurinavichius, K.S., Suzina, N.E., Osipov, G.A., Lysenko, A.M., Gilichinsky, D.A., and Akimenko, V.K., Novel psychrophilic anaerobic spore-forming bacterium from the overcooled water brine in permafrost: Description Clostridium algoriphilum sp. nov., Extremophiles, 2005, vol. 9, pp. 239–246.

    Article  Google Scholar 

  • Shcherbakova, V., Rivkina, E., Laurinavichuis, K., Pecheritsina, S., and Gilichinsky, D., Physiological characteristics of bacteria isolated from water brines within permafrost, Int. J. Astrobiol., 2004, vol. 3, no. 1, pp. 37–43.

    Article  Google Scholar 

  • Shivaji, S., Kumari, K., Kishore, K.H., Pindi, P.K., Rao, P.S., Radha Srinivas, T.N., Asthana, R., and Ravindra R., Vertical distribution of bacteria in a lake sediment from Antarctica by culture-independent and culturedependent approaches, Res. Microbiol., 2011, vol. 162, no. 2, pp. 191–203.

    Article  Google Scholar 

  • Shivaji, S., Begum, Z., Shiva Nageswara Rao, S.S., VishnuVardhan Reddy, P.V., Manasa, P., Sailaja, B., Prathiba, M.S., Thamban, M., Krishnan, K.P., Singh, S.M., and Srinivas, T.N., Antarctic ice core samples: Culturable bacterial diversity, Res. Microbiol., 2013, vol. 164, no. 1, pp. 70–82.

    Article  Google Scholar 

  • Tamura, K., Stecher, G., Peterson, D., Filipski, A., and Kumar, S., MEGA6: Molecular evolutionary genetics analysis version 6.0, Mol. Biol. Evol., 2013, vol. 30, no. 12, pp. 2725–2729.

    Article  Google Scholar 

  • Thompson, J.D., Higgins, D.G., and Gibson, T.J., CLUSTAL W: Improving the sensitivity of progressive multiple sequence alignment through sequence weighting, positions- specific gap penalties and weight matrix choice, Nucl. Acids Res., 1994, vol. 22, pp. 4673–4680.

    Article  Google Scholar 

  • Trofimov, V.T., Badu, Yu.B., and Kudryashov, V.G., Poluostrov Yamal (inzhenerno-geologicheskii ocherk) (Yamal Peninsula: Engineering–Geological Sketch), Trofimov, V.T., Ed., Moscow: Mosk. Gos. Univ., 1975.

    Google Scholar 

  • Trujillo, M.E., Willems, A., Abril, A., Planchuelo, A.-M., Rivas, R., Ludena, D., Mateos, P.F., Martinez-Molina, E., and Velazquez, E., Nodulation of Lupinus albus by strains of Ochrobactrum lupini sp. nov., Appl. Environ. Microbiol., 2005, vol. 71, no. 3, pp. 1318–1327.

    Article  Google Scholar 

  • Vu, B., Chen, M., Crawford, R.J., and Ivanova, E., Bacterial extracellular polysaccharides involved in biofilm formation, Molecules, 2009, vol. 14, no. 7, pp. 2535–2554.

    Article  Google Scholar 

  • Weisburg, W.G., Barns, S.M., Pelletier, D.A., and Lane, D.J., 16S ribosomal DNA amplification for phylogenetic study, J. Bacteriol., 1991, vol. 173, no. 2, pp. 697–703.

    Article  Google Scholar 

  • Yoshikawa, K., Romanovsky, V., Duxbury, N., Browna, J., and Tsapin, A., The use of geophysical methods to discriminate between brine lavers and freshwater taliks in permafrost regions, J. Glaciol. Geocryol., 2004, vol. 26, pp. 220–230.

    Google Scholar 

  • Yu, X., Li, Y., Zhang, C., Liu, H., Liu, J., Zheng, W., Kang, X., Leng, X., Zhao, K., Gu, Y., Zhang, X., Xiang, Q., and Chen, Q., Culturable heavy metal-resistant and plant growth promoting bacteria in V-Ti magnetite mine tailing soil from Panzhihua, China, PLoS One, 2014, vol. 9, no. 9, pp. 1–9.

    Google Scholar 

  • Zlamala, C., Schumann, P., Kampfer, P., Valens, M., Rossello-Mora, R., Lubitz, W., and Busse, H.J., Microbacterium aerolatum sp. nov., isolated from the air in the “Virgilkapelle” in Vienna, Int. J. Syst. Evol. Microbiol., 2002, vol. 52, no. 4, pp. 1229–1234.

    Google Scholar 

  • Zurdo-Pineiro, J.L., Rivas, R., Trujillo, M.E., Vizcaino, N., Carrasco, J.A., Chamber, M., Palomares, A., Mateos, P.F., Martinez-Molina, E., and Velazquez, E., Ochrobactrum cytisi sp. nov., isolated from nodules of Cytisus scoparius in Spain, Int. J. Syst. Evol. Microbiol., 2007, vol. 57, no. 4, pp. 784–788.

    Article  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to E. V. Spirina.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Spirina, E.V., Durdenko, E.V., Demidov, N.E. et al. Halophilic-psychrotrophic bacteria of an Alaskan cryopeg—a model for astrobiology. Paleontol. J. 51, 1440–1452 (2017). https://doi.org/10.1134/S0031030117120036

Download citation

  • Received:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S0031030117120036

Keywords

Navigation