Skip to main content
SpringerLink
Log in

Microeukaryotes in the Metagenomes of Late Pleistocene Permafrost Deposits

  • Published:
Paleontological Journal Aims and scope Submit manuscript

Abstract—

The analysis of metagenomes from four Late Pleistocene permafrost samples allowed us to recognize nearly four hundred genera of protists and fungi, as well as nematodes, in the microeukaryotic assemblage. The sample of the ancient oxbow lake sediments is characterized by the highest taxonomic diversity. Heterotrophic protists and autotrophs dominated the deposits that formed under hydromorphic conditions. Fungi, in turn, prevailed in the Ice Complex deposits. In general, metagenomic analysis characterizes the assemblages from permafrost deposits more entirely than the standard methods of enrichment cultivation.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1.
Fig. 2.

Similar content being viewed by others

REFERENCES

  1. Adl, S.M., Bass, D., Lane, C.E., Lukeš, J., Schoch, C.L., Smirnov, A., Agatha, S., Berney, C., Brown, M.W., Burki, F., Cárdenas, P., Čepička, I., Chistyakova, L., and Campo, J. del, Dunthorn, M., Edvardsen, B., Eglit, Y., Guillou, L., et al., Revisions to the classification, nomenclature, and diversity of eukaryotes, J. Eukar. Microbiol., 2019, vol. 66, pp. 4–119.

    Article  Google Scholar 

  2. Arndt, D., Xia, J., Liu, Y., Zhou, Y., Guo, A.C., Cruz, J.A., Sinelnikov, I., Budwill, K., Nesbo, C.L., and Wishart, D.S., METAGENassist: a comprehensive web server for comparative metagenomics, Nucleic Acid Res., 2012, vol. 40, no. W1, pp. W88–W95.

    Article  Google Scholar 

  3. Berney, C., Geisen, S., Van Wichelen, J., Nitsche, F., Vanormelingen, P., Bonkowski, M., and Bass, D., Expansion of the “reticulosphere”: diversity of novel branching and network-forming amoebae helps to define Variosea (Amoebozoa), Protist, 2015, vol. 166, pp. 271–295.

    Article  Google Scholar 

  4. Bohmann, K., Evans, A., Gilbert, M.T.P., Carvalho, G.R., Creer, S., Knapp, M., Yu, D.W., and De Bruyn, M., Environmental DNA for wildlife biology and biodiversity monitoring, Trends Ecol. Evol., 2014, vol. 29, no. 6, pp. 358–367.

    Article  Google Scholar 

  5. Bolshiyanov, D.Yu., Grigor’ev, M.N., Shnaider, V., Makarov, A.S., and Gusev E.A., Sea-level fluctuations, and Ice Complex formation on the Laptev Sea coast during the Late Pleistocene, in Sistema morya Laptevykh i prilegayushchikh morei Arktiki: sovremennoe sostoyanie i istoriya razvitiya (System of the Laptev Sea and the Adjacent Arctic Seas: Modern and Past Environments), 2009, Moscow: Mosk. Gos. Univ., pp. 349–356.

  6. Bonkowski, M., Protozoa and plant growth: the microbial loop in soil revisited, New Phytol., 2004, vol. 162, no. 3, pp. 617–631.

    Article  Google Scholar 

  7. Briar, S.S., Fonte, S.J., Park, I., Six, J., Scow, K., and Ferris, H., The distribution of nematodes and soil microbial communities across soil aggregate fractions and farm management systems, Soil Biol. Biochem., 2011, vol. 43, no. 5, pp. 905–914.

    Article  Google Scholar 

  8. Culligan, E.P. and Sleator, R.D., Editorial: from genes to species: Novel insights from metagenomics, Front. Microbiol., 2016, vol. 7.

  9. Demidov, N.E., Baranskaya, A.V., Durdenko, E.V., Zanina, O.G., Karaevskaya, E.S., Pushina, Z.V., Rivkina, E.M., Spirina, E., and Spenser, R., Biogeochemistry of permanently frozen deposits on the arctic shore of Gydan peninsula, Arctic Antarctic Res., 2016, vol. 3, pp. 34–49.

    Google Scholar 

  10. Dmitriev, V.V., Gilichinskii, D.A., Faizutdinova, R.N., Shershunov, I.N., Golubev, V.I., and Duda, V.I., Detection of viable yeast in 3-million-year-old permafrost soils of Siberia, Microbiology, 1997, vol. 66, no. 5, pp. 655–660.

    Google Scholar 

  11. Domonell, A., Brabender, M., Nitsche, F., Bonkowski, M., and Arndt, H., Community structure of cultivable protists in different grassland and forest soils of Thuringia, Pedobiologia, 2013, vol. 56, no. 1, pp. 1–7.

    Article  Google Scholar 

  12. Dupont, A.O.C., Griffiths, R.I., Bell, T., and Bass, D., Differences in soil micro-eukaryotic communities over soil pH gradients are strongly driven by parasites and saprotrophs: Soil pH and protistan diversity, Environ Microbiol., 2016, vol. 18, no. 6, pp. 2010–2024.

    Article  Google Scholar 

  13. Faizutdinova, R.N., Suzina, N.E., Duda, V.I., Petrovskaya, L.E., and Gilichinsky, D.A., Yeasts isolated from ancient permafrost in Life in Ancient Ice, 2005. Princeton: Princeton Univ. Press, 2005, pp. 118–126.

    Google Scholar 

  14. Finlay, B.J., Black, H.I.J., Brown, S., Clarke, K.J., Esteban, G.F., Hindle, R.M., Olmo, J.L., Rollett, A., and Vickerman, K., Estimating the growth potential of the soil protozoan community, Protist, 2000, vol. 151, no. 1, pp. 69–80.

    Article  Google Scholar 

  15. Geisen, S., Bandow, C., Römbke, J., and Bonkowski, M., Soil water availability strongly alters the community composition of soil protists, Pedobiologia, 2014, vol. 57, nos. 4–6, pp. 205–213.

    Article  Google Scholar 

  16. Geisen, S., Tveit, A.T., Clark, I.M., Richter, A., Svenning, M.M., Bonkowski, M., and Urich, T., Metatranscriptomic census of active protists in soils, ISME J., 2015, vol. 9, no. 10, pp. 2178–2190.

    Article  Google Scholar 

  17. Gilichinsky, D.A. and Rivkina, E.M., Permafrost microbiology, in Encyclopedia of Geobiology, 2011. Encyclopedia of Earth Sciences Series, Reitner, J. and Thiel, V., Springer Netherlands, 2011, pp. 726–732.

  18. Gilichinsky, D., Khlebnikova, G., Zvyagintsev, D., Fyodorov-Davydov, D., and Kudryavtseva, N., Microbiological characterization by studying sedimentary deposits of cryolithozone, Izv. Akad. Nauk SSSR, Ser. Geol., 1989, vol. 6, pp. 103–115.

    Google Scholar 

  19. Gubin, S.V., Lupachev, A.V., Shatilovich, A.V., Myl’nikov, A.P., Ryss, A.Yu., Veremeeva, A.A., The influence of cryogenic mass exchange on the distribution of viable microfauna in cryozems, Pochvovedenie, 2016, vol. 12, pp. 1485–1499.

    Google Scholar 

  20. Jacquiod, S., Stenbæk, J., Santos, S.S., Winding, A., Sørensen, S.J., and Priemé, A., Metagenomes provide valuable comparative information on soil microeukaryotes, Res. Microbiol., 2016, vol. 167, no. 5, pp. 436–450.

    Google Scholar 

  21. Kochkina, G.A., Ivanushkina, N.E., Karasev, S.G., Gavrish, E.Y., Gurina, L.V., Evtushenko, L.I., Spirina, E.V., Vorob’eva, E.A., Gilichinskii, D.A., and Ozerskaya, S.M., Survival of micromycetes and actinobacteria under conditions of long-term natural cryopreservation, Microbiology, 2001, vol. 70, no. 3, pp. 356–364.

    Article  Google Scholar 

  22. Lewin, A., Wentzel, A., and Valla, S., Metagenomics of microbial life in extreme temperature environments, Curr. Opin. Biotechnol., 2013, vol. 24, no. 3, pp. 516–525.

    Article  Google Scholar 

  23. Lindahl, T., Instability and decay of the primary structure of DNA, Nature, 1993, vol. 362, no. 6422.

  24. Malavin, S. and Shmakova, L., Microeukaryotes in metagenomic survey of ancient Siberian permafrost. Institute of Physicochemical and Biological Problems in Soil Science RAS. Sampling event dataset. 2020. https://doi.org/ accessed via GBIF.org on 2020-04-15.https://doi.org/10.15468/wtkvuu

  25. Mackelprang, R., Waldrop, M.P., DeAngelis, K.M., David, M.M., Chavarria, K.L., Blazewicz, S.J., Rubin, E.M., and Jansson, J.K., Metagenomic analysis of a permafrost microbial community reveals a rapid response to thaw, Nature, 2011, vol. 480, no. 7377, pp. 368–371.

    Article  Google Scholar 

  26. Meyer, F., Paarmann, D., D’Souza, M., Olson, R., Glass, E., Kubal, M., Paczian, T., Rodriguez, A., Stevens, R., Wilke, A., Wilkening, J., and Edwards, R., The metagenomics RAST server—a public resource for the automatic phylogenetic and functional analysis of metagenomes, BMC Bioinformatics, 2008, vol. 9, no. 1.

  27. Pawlowski, J., Protist Evolution and Phylogeny, (eLS), Chichester, UK: John Wiley, Ltd, 2014.

    Google Scholar 

  28. Quast, C., Pruesse, E., Yilmaz, P., Gerken, J., Schweer, T., Yarza, P., Peplies, J., and Glöckner, F.O., The SILVA ribosomal RNA gene database project: improved data processing and web-based tools, Nucleic Acid Res., 2013, vol. 41, no. D1, pp. D590–D596.

    Article  Google Scholar 

  29. Rivkina, E., Petrovskaya, L., Vishnivetskaya, T., Krivushin, K., Shmakova, L., Tutukina, M., Meyers, A., and Kondrashov, F., Metagenomic analyses of the late Pleistocene permafrost—additional tools for reconstruction of environmental conditions, Biogeosciences, 2016, vol. 13, no. 7, pp. 2207–2219.

    Article  Google Scholar 

  30. Rivkina, E., Abramov, A., Spirina, E., Petrovskaya, L., Shatilovich, A., Shmakova, L., Scherbakova, V., and Vishnivetskaya, T., Earth’s perennially frozen environments as a model of cryogenic planet ecosystems, Permafrost and Periglacial Processes, 2018, vol. 29, no. 4, pp. 246–256.

    Article  Google Scholar 

  31. Schirrmeister, L., Kunitsky, V., Grosse, G., Wetterich, S., Meyer, H., Schwamborn, G., Babiy, O., Derevyagin, A., and Siegert, C., Sedimentary characteristics and origin of the Late Pleistocene Ice Complex on north-east Siberian Arctic coastal lowlands and islands – A review, Quat. Int., 2011, vol. 241, no. 1, pp. 3–25.

    Article  Google Scholar 

  32. Shatilovich, A.V., Shmakova, L.A., Gubin, S.V., and Gilichinskii, D.A., Viable protists from the Arctic permafrost, Earth’s Cryosphere, 2010, vol. 14, no. 2, pp. 69–78.

    Google Scholar 

  33. Shatilovich, A.V., Chesunov, A.V., Neretina, T.V., Grabarnik, I.P., Gubin, S.V., Vishnivetskaya, T.A., Onstott, T.S., and Rivkina, E.M., Viable Nematodes from Late Pleistocene Permafrost of the Kolyma River Lowland, Dokl. Earth Sci., 2018, vol. 480, no. 1, pp. 100–102.

    Google Scholar 

  34. Shi, T., Reeves, R.H., Gilichinsky, D.A., and Friedmann, E.I., Characterization of viable bacteria from Siberian permafrost by 16S rDNA sequencing, Microb. Ecol., 1997, vol. 33, no. 3, pp. 169–179.

    Article  Google Scholar 

  35. Shmakova, L.A. and Rivkina, E.M., Viable eukaryotes of the phylum Amoebozoa from the Arctic permafrost, Paleontol. J., 2015, vol. 49, no. 6, pp. 572–577.

    Article  Google Scholar 

  36. Shmakova, L.A., Fedorov-Davydov, D.G., and Rivkina, E.M., Amoeboid protists from cryogenic soils in the Kolyma Lowland, Pochvovedenie, 2014, no. 1, pp. 91–99.

  37. Shmakova, L., Bondarenko, N., and Smirnov, A., Viable species of Flamella (Amoebozoa: Variosea) isolated from ancient arctic permafrost sediments, Protist, 2016, vol. 167, no. 1, pp. 13–30.

    Article  Google Scholar 

  38. Shmakova, L.A., Karpov, S.A., Malavin, S.A., and Smirnov, A.V., Morphology, biology and phylogeny of Phalansterium arcticum sp. n. (Amoebozoa, Variosea), isolated from ancient Arctic permafrost, Eur. J. Protistol., 2018.

  39. Smirnov, A.V., Chao, E., Nassonova, E.S., and Cavalier-Smith, T., A revised classification of naked lobose amoebae (Amoebozoa: Lobosa), Protist, 2011, vol. 162, no. 4, pp. 545–570.

    Article  Google Scholar 

  40. Tikhonenkov, D.V., Mazei, Yu.A., and Embulaeva, E.A., The species composition and structure of the heterotrophic flagellates in forest-steppe soils of the Middle Volga River basin, Eur. Soil. Sci., 2011, vol. 44, no. 2, pp. 194–203.

    Article  Google Scholar 

  41. Tveit, A., Schwacke, R., Svenning, M.M., and Urich, T., Organic carbon transformations in high-Arctic peat soils: key functions and microorganisms, The ISME J., 2013, vol. 7, no. 2, pp. 299–311.

    Article  Google Scholar 

  42. Venter, P.C., Nitsche, F., Domonell, A., Heger, P., and Arndt, H., The protistan microbiome of grassland soil: Diversity in the mesoscale, Protist, 2017, vol. 168, no. 5, pp. 546–564.

    Article  Google Scholar 

  43. Vishnivetskaya, T.A., Viable cyanobacteria and green algae from the permafrost darkness, in Permafrost Soils, Margesin, R. Ed., Berlin, Heidelberg: Springer Berlin Heidelberg, 2009, vol. 16, pp. 73–84.

    Google Scholar 

  44. Wooley, J.C., Godzik, A., and Friedberg, I., A primer on metagenomics, PLoS Comp. Biol., 2010, vol. 6, no. 2, p. e1000667.

    Article  Google Scholar 

  45. Wu, S., Zhu, Z., Fu, L., Niu, B., and Li, W., WebMGA: a customizable web server for fast metagenomic sequence analysis, BMC Genomics, 2011, vol. 12, no. 1.

  46. Yergeau, E., Hogues, H., Whyte, L.G., and Greer, C.W., The functional potential of high Arctic permafrost revealed by metagenomic sequencing, qPCR and microarray analyses, The ISME J., 2010, vol. 4, no. 9, pp. 1206–1214.

    Article  Google Scholar 

Download references

Funding

This paper was prepared within the framework of the State assignment 0191-2019-0044. The investigations were supported by the Russian Foundation for Basic Research (projects nos. 17-54-150003, 18-04-00824, 19-04-01240, 19-29-05003mk), as well as KP19-274 and KP19-280.

Author information

Authors and Affiliations

  1. Institute of Physicochemical and Biological Problems in Soil Science (IPCBPSS RAS), 142290, Pushchino, Moscow oblast, Russia

    L. A. Shmakova, S. A. Malavin, E. V. Spirina & E. M. Rivkina

  2. Institute of Cell Biophysics of the Russian Academy of Sciences, 142290, Pushchino, Moscow oblast, Russia

    M. N. Tutukina

Authors
  1. L. A. Shmakova
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. S. A. Malavin
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. E. V. Spirina
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. M. N. Tutukina
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. E. M. Rivkina
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to L. A. Shmakova.

Additional information

Translated by D. Voroshchuk

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Shmakova, L.A., Malavin, S.A., Spirina, E.V. et al. Microeukaryotes in the Metagenomes of Late Pleistocene Permafrost Deposits. Paleontol. J. 54, 913–921 (2020). https://doi.org/10.1134/S003103012008016X

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S003103012008016X

Keywords:

Search

Navigation