Microbial Communities of Interglacial and Interstadial Paleosols of the Late Pleistocene

Abstract

The taxonomic structure of microbial communities in the Late Pleistocene paleosols of different ages in the Central Russian Upland formed under contrasting climatic conditions were analyzed. The humic horizons of paleosols in the interstadial periods of the Early Valdai (105–95 kyr ago), Middle Valdai (33–24 kyr ago), Mikulino interglacial (130–117 kyr ago), and of the modern (Holocene) chernozem were considered. Microbial DNA was analyzed using quantitative PCR and 16S rRNA gene amplicon sequencing (DNA metabarcoding). The numbers of copies of archaeal, bacterial, and fungal genes gradually decreased with an increase in the soil age. All considered paleosols significantly differed from one another in the structure of their microbial communities. The Verrucomicrobia-to-Nitrospirae ratio was used as a diagnostic parameter reflecting the organic matter supply and the changes in carbon and nitrogen cycles. The Verrucomicrobia-to-Nitrospirae ratio in the interstadial soils was 140–200 times lower as compared with that in the modern soil (typical chernozem) and in the paleosols of the Mikulino interglacial. The share of gram-negative Proteobacteria and Acidobacteria increased with the soil age, whereas the share of gram-positive Actinobacteria and Firmicutes decreased. The modern chernozems and interglacial paleosols were characterized by similar values of microbial diversity, while the paleosols of the Valdai interstadial had significantly lower microbial diversity and species richness. Analysis of β-diversity showed that the paleosols of different types and ages maintained the difference in the structure and diversity of their microbial communities depending on the conditions of their formation. Thus, the microbial communities can be used as potential stratigraphic markers and indicators of different climatic conditions, under which the given paleosols were formed.

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REFERENCES

  1. 1

    T. A. Arkhangel’skaya, M. V. Prokhorov, and M. A. Mazirov, “Annual dynamics of arable soils of paleocryogenic complexes of Vladimir Opol’e,” Kriosfera Zemli, No. 3, 80–86 (2008).

    Google Scholar 

  2. 2

    E. V. Blagodatskaya, O. S. Khokhlova, T.-H. Anderson, and S. A. Blagodatskii, “Extractable microbial DNA pool and microbial activity in paleosols of Southern Urals,” Microbiology (Moscow) 72, 750–755 (2003).

    Article  Google Scholar 

  3. 3

    E. V. Blagodatskaya, M. V. Semenov, and A. V. Yakushev, Activity and Biomass of Soil Microorganisms under Conditions of Changing Environment (KMK, Moscow, 2016) [in Russian].

    Google Scholar 

  4. 4

    A. V. Borisov, T. S. Demkina, and V. A. Demkin, P-aleosols and Climate of Yergeni in the Bronze Age (4th–2nd Centuries BC) (Nauka, Moscow, 2006) [in Russian].

    Google Scholar 

  5. 5

    A. A. Velichko and T. D. Morozova, Climate and Landscapes of Northern Eurasia under Global Warming: Retrospective Analysis and Scenarios (GEOS, Moscow, 2010), pp. 120–127.

    Google Scholar 

  6. 6

    V. A. Demkin, N. N. Kashirskaya, T. S. Demkina, T. E. Khomutova, and M. V. El’tsov, “Paleosol studies of burial mounds in the Ilovlya River valley (the Privolzhskaya Upland),” Eurasian Soil Sci. 41, 115–127 (2008).

    Article  Google Scholar 

  7. 7

    V. A. Demkin, A. V. Borisov, T. S. Demkina, T. E. Khomutova, B. N. Zolotareva, N. N. Kashirskaya, and E. V. Demkina, “Steppe pyramids of Eurasia: unique archive of Holocene paleosols,” in Paleosols and Indicators of Continental Weathering in the History of Biosphere (Paleontological Institute, Russian Academy of Sciences, Moscow, 2010), pp. 132–163.

    Google Scholar 

  8. 8

    T. S. Demkina, T. E. Khomutova, N. N. Kashirskaya, I. V. Stretovich, and V. A. Demkin, “Microbiological investigations of paleosols of archeological monuments in the steppe zone,” Eurasian Soil Sci. 43, 194‒201 (2010).

    Article  Google Scholar 

  9. 9

    T. S. Demkina, T. E. Khomutova, N. N. Kashirskaya, I. V. Stretovich, and V. A. Demkin, “Characteristics of microbial communities in steppe paleosols buried under kurgans of the Sarmatian time (I–IV centuries AD),” Eurasian Soil Sci. 42, 778–793 (2009).

    Article  Google Scholar 

  10. 10

    I. V. Ivanov, L. S. Pesochina, and V. M. Semenov, “Biological mineralization of organic matter in the modern virgin and plowed chernozems, buried chernozems, and fossil chernozems,” Eurasian Soil Sci. 42, 1109–1119 (2009).

    Article  Google Scholar 

  11. 11

    A. O. Makeev, “Ecological role of paleosols in geological history,” in Soils in the Biosphere and Human Life (Moscow State Univ., Moscow, 2012), pp. 183–283.

    Google Scholar 

  12. 12

    O. E. Marfenina, D. S. Sakharov, A. E. Ivanova, and A. V. Rusakov, “Mycological complexes in Holocene and Late Pleistocene paleohorizons and in fragments of paleosols,” Eurasian Soil Sci. 42, 432–439 (2009).

    Article  Google Scholar 

  13. 13

    T. D. Morozova, Development of Soil Cover of Europe in Late Pleistocene (Nauka, Moscow, 1981) [in Russian].

    Google Scholar 

  14. 14

    Guide for Scientific Field Excursions of the VII Congress of Dokuchaev Soil Society and All-Russian Scientific Conference with International Participation “Soil Science for Food and Ecological Safety of the Country,” Belgorod, August 15–22, 2010 (Moscow, 2016) [in Russian].

  15. 15

    P. R. Pushkina and S. A. Sycheva, “Paleosols in depressions of the Central Russian Upland in the Early Valdai Time,” Eurasian Soil Sci. 47, 371–380 (2014). https://doi.org/10.1134/S1064229314050202

    Article  Google Scholar 

  16. 16

    A. V. Rusakov and V. V. Novikov, “Biological activity in modern and buried soils of the historical center of St. Petersburg,” Microbiology (Moscow) 72, 103–109 (2003).

    Article  Google Scholar 

  17. 17

    S. A. Sycheva, “Evolutionary analysis of Pleistocene of buried small erosion forms,” Geomorfologiya, No. 3, 31–38 (1996).

    Google Scholar 

  18. 18

    S. A. Sycheva and V. S. Gunova, “Analysis results of Late Pleistocene loess-soil complex in buried balka ystem of the Central Russian Upland,” Byull. Kom. Izuch. Chetvertichn. Perioda, Akad. Nauk SSSR, No. 65, 86–101 (2004).

    Google Scholar 

  19. 19

    S. A. Sycheva, “Late Pleistocene permafrost phenomena in periglacial area of the Russian Plain and their relation with paleosols,” in Problems of Paleogeography and Stratigraphy of Pleistocene (Moscow State Univ., Moscow, 2011), No. 3, pp. 228–237.

  20. 20

    T. E. Khomutova, T. S. Demkina, and V. A. Demkin, “Estimation of the total and active microbial biomasses in buried subkurgan paleosoils of different ages,” Microbiology (Moscow) 73, 196–201 (2004).

    Article  Google Scholar 

  21. 21

    T. E. Khomutova, T. S. Demkina, A. V. Borisov, and I. I. Shishlina, State of microbial communities in paleosols buried under kurgans of the desert-steppe zone in the Middle Bronze Age (27th–26th centuries BC) in relation to the dynamics of climate humidity, Eurasian Soil Sci. 50, 229–238 (2017). https://doi.org/10.1134/S1064229317020065

    Article  Google Scholar 

  22. 22

    T. I. Chernov, A. D. Zheleznova, O. V. Kutovaya, A. O. Makeev, A. K. Tkhakakhova, N. A. Bgazhba, F. G. Kurbanova, A. V. Rusakov, T. A. Puzanova, and O. S. Khokhlova, “Comparative analysis of the structure of buried and surface soils by analysis of microbial DNA Microbiology (Moscow) 87, 833–841 (2018).

  23. 23

    T. H. Anderson, “Microbial eco-physiological indicators to asses soil quality,” Agric., Ecosyst. Environ. 98 (1–3), 285–293 (2003).

    Article  Google Scholar 

  24. 24

    E. Aseyeva, A. Makeev, F. Kurbanova, P. Kust, A. Rusakov, O. Khokhlova, E. Mihailov, T. Puzanova, and A. Golyeva, “Paleolandscape reconstruction based on the study of a buried soil of the bronze age in the broadleaf forest area of the Russian Plain,” Geosciences 9 (3), 111 (2019).

    Article  Google Scholar 

  25. 25

    G. T. Bergmann, S. T. Bates, K. G. Eilers, C. L. Lauber, J. G. Caporaso, W. A. Walters, R. Knight, and N. Fierer, “The under-recognized dominance of Verrucomicrobia in soil bacterial communities,” Soil Biol. Biochem. 43 (7), 1450–1455 (2011).

    Article  Google Scholar 

  26. 26

    J. G. Caporaso, J. Kuczynski, J. Stombaugh, K. Bittinger, F. D. Bushman, E. K. Costello, N. Fierer, A. Gonzalez Peña, et al., “QIIME allows analysis of high-throughput community sequencing data,” Nat. Methods 7 (5), 335 (2010).

    Article  Google Scholar 

  27. 27

    J. G. Caporaso, C. L. Lauber, W. A. Walters, D. Berg-Lyons, J. Huntley, N. Fierer, S. M. Owens, et al., “Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms,” ISME J. 6, 1621−1624 (2012).

    Article  Google Scholar 

  28. 28

    U. N. da Rocha, F. D. Andreote, J. L. de Azevedo, J. D. van Elsas, and L. S. van Overbeek, “Cultivation of hitherto-uncultured bacteria belonging to the Verrucomicrobia subdivision 1 from the potato (Solanum tuberosum L.) rhizosphere,” J. Soil Sediment. 10, 326–339 (2010).

    Article  Google Scholar 

  29. 29

    K. G. Eilers, S. Debenport, S. Anderson, and N. Fierer, “Digging deeper to find unique microbial communities: the strong effect of depth on the structure of bacterial and archaeal communities in soil,” Soil Biol. Biochem. 50, 58–65 (2012).

    Article  Google Scholar 

  30. 30

    N. Fierer, J. Ladau, J. C. Clemente, J. W. Leff, S. M. Owens, K. S. Pollard, R. Knight, J. A. Gilbert, and R. L. McCulley, “Reconstructing the microbial diversity and function of pre-agricultural tallgrass prairie soils in the United States,” Science 342, 621–624 (2013).

    Article  Google Scholar 

  31. 31

    P. H. Janssen, “Pathway of glucose catabolism by strain VeGlc2, an anaerobe belonging to the Verrucomicrobiales lineage of bacterial descent,” Appl. Environ. Microbiol. 64, 4830–4833 (1998).

    Article  Google Scholar 

  32. 32

    O. Koch, D. Tscherko, and E. Kandeler, “Temperature sensitivity of microbial respiration, nitrogen mineralization, and potential soil enzyme activities in organic alpine soils,” Global Biogeochem. Cycles 21, GB4017 (2007).

    Article  Google Scholar 

  33. 33

    H. Koch, S. Lücker, M. Albertsen, K. Kitzinger, C. Herbold, E. Spieck, P. H. Nielsen, M. Wagner, and H. Daims, “Expanded metabolic versatility of ubiquitous nitrite-oxidizing bacteria from the genus Nitrospira,” Proc. Natl. Acad. Sci. U.S.A. 112 (36), 11371–11376 (2015).

    Article  Google Scholar 

  34. 34

    I. Kovda, S. Sycheva, M. Lebedeva, and S. Inozemtzev, “Variability of carbonate pedofeatures in a loess-paleosol sequence and their use for paleoreconstructions,” J. Mt. Sci. 6 (2), 155–161 (2009).

    Article  Google Scholar 

  35. 35

    C. Lozupone, M. E. Lladser, D. Knights, J. Stombaugh, and R. Knight, “UniFrac: an effective distance metric for microbial community comparison,” ISME J. 5 (2), 169 (2011).

    Article  Google Scholar 

  36. 36

    S. Lücker, M. Wagner, F. Maixner, E. Pelletier, H. Koch, B. Vacherie, T. Rattei, J. S. Sinninghe Damsté, E. Spieck, D. Le Paslier, and H. Daims, “A Nitrospira metagenome illuminates the physiology and evolution of globally important nitrite-oxidizing bacteria,” Proc. Natl. Acad. Sci. U.S.A. 107 (30), 13479–13484 (2010).

    Article  Google Scholar 

  37. 37

    W. E. Lukens, L. C. Nordt, G. E. Stinchcomb, S. G. Driese, and J. D. Tubbs, “Reconstructing pH of paleosols using geochemical proxies,” J. Geol. 126 (4), 427–449 (2018).

    Article  Google Scholar 

  38. 38

    A. Makeev, P. Kust, M. Lebedeva, A. Rusakov, B. Terhorst, and T. Yakusheva, “Soils in the bipartite sediments within the Moscow glacial limits of the Russian Plain: sedimentary environment, pedogenesis, paleolandscape implication,” Quart. Int. 501, 147–173 (2017).

    Article  Google Scholar 

  39. 39

    A. Makeev, E. Aseeva, A. Rusakov, K. Sorokina, T. Puzanova, O. Khokhlova, P. Kust, F. Kurbanova, T. Chernov, O. Kutovaya, M. Lebedeva, and E. Mihailov, “The environment of the Early Iron Age at the southern fringe of the forest zone of the Russian Plain,” Quart. Int. 502, 218–237 (2019).

    Article  Google Scholar 

  40. 40

    A. A. Navarrete, T. Soares, R. Rossetto, J. A. van Veen, S. M. Tsai, and E. E. Kuramae, “Verrucomicrobial community structure and abundance as indicators for changes in chemical factors linked to soil fertility,” Antonie Leeuwenhoek 108 (3), 741–752 (2015).

    Article  Google Scholar 

  41. 41

    B. Nowka, H. Daims, and E. Spieck, “Comparison of oxidation kinetics of nitrite-oxidizing bacteria: nitrite availability as a key factor in niche differentiation,” Appl. Environ. Microbiol. 81 (2), 745–753 (2015).

    Article  Google Scholar 

  42. 42

    A. Rusakov, A. Makeev, O. Khokhlova, P. Kust, M. Lebedeva, T. Chernov, A. Golyevae, A. Popova, F. Kurbanova, and T. Puzanova, “Palaeoenvironmental reconstruction based on soils buried under Scythian fortification in the southern forest-steppe area of the East European Plain,” Quart. Int. 502, 197–217 (2019).

    Article  Google Scholar 

  43. 43

    M. V. Semenov, T. I. Chernov, A. K. Tkhakakhova, A. D. Zhelezova, E. A. Ivanova, T. V. Kolganova, and O. V. Kutovaya, “Distribution of prokaryotic communities throughout the chernozem profiles under different land uses for over a century,” Appl. Soil Ecol. 127, 8–18 (2018).

    Article  Google Scholar 

  44. 44

    I. V. Senechkin, A. G. C. L. Speksnijder, A. M. Semenov, A. H. C. van Bruggen, and L. S. van Overbeek, “Isolation and partial characterization of bacterial strains on low organic carbon medium from soils fertilized with different organic amendments,” Microb. Ecol. 60, 829–839 (2010).

    Article  Google Scholar 

  45. 45

    S. Sycheva and O. Khokhlova, “Genesis, 14C-age and duration of development of the Bryansk paleosol on the Central Russian upland on dating of different materials,” Quart. Int. 399, 111–121 (2016).

    Article  Google Scholar 

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Funding

This study was supported by the Russian Science Foundation (project no. 17-16-01057).

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Correspondence to M. V. Semenov.

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Translated by G. Chirikova

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Semenov, M.V., Chernov, T.I., Zhelezova, A.D. et al. Microbial Communities of Interglacial and Interstadial Paleosols of the Late Pleistocene. Eurasian Soil Sc. 53, 772–779 (2020). https://doi.org/10.1134/S1064229320060101

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Keywords:

  • soil memory
  • microbiome
  • DNA metabarcoding
  • quantitative PCR
  • microbial diversity