Skip to main content
Log in

Distribution of Metabolically Active Prokaryotes (Archaea and Bacteria) throughout the Profiles of Chernozem and Brown Semidesert Soil

  • Soil Biology
  • Published:
Eurasian Soil Science Aims and scope Submit manuscript

Abstract

The distribution of metabolically active cells of archaea and bacteria in the profiles of typical chernozems (Voronezh oblast) and brown semidesert soils (Astrakhan oblast) of natural and agricultural ecosystems was studied using the method of fluorescent in situ hybridization (FISH). The studied soils differed sharply in the microbial biomass and in the numbers of metabolically active cells of archaea and bacteria. The number of active bacterial cells was 3.5–7.0 times greater than that of archaea. In the arable chernozem, the numbers of active cells of archaea and bacteria were 2.6 and 1.5 times, respectively, lower than those in the chernozem under the shelterbelt. The agricultural use of the brown semidesert soil had little effect on the abundances of bacteria and archaea. The soil organic carbon content was the major factor controlling the numbers of metabolically active cells of both domains. However, the dependence of the abundance of bacteria on the organic matter content was more pronounced. The decrease in the organic carbon and total nitrogen contents down the soil profiles was accompanied by the decrease in the bacteria: archaea ratio attesting to a better adaptation of archaea to the permanent deficiency of carbon and nitrogen. The bacteria: archaea ratio can serve as an ecotrophic indicator of the state of soil microbial communities.

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

  1. Unified State Register of Soil Resources of Russia, Version 1.0 (Dokuchaev Soil Sciences Institute, Moscow, 2014) [in Russian].

  2. N. A. Manucharova, Identification of Metabolically Active Prokaryotic Cells in Soils Using in Situ Molecular-Biological Fluorescence Hybridization (FISH) (Universitet i Shkola, Moscow, 2008) [in Russian].

    Google Scholar 

  3. N. A. Manucharova, A. N. Vlasenko, D. G. Zvyagintsev, and E. V. Men’ko, “Specificity of the chitinolytic microbial complex of soils incubated at different temperatures,” Microbiology (Moscow) 80 (2), 205–215 (2011).

    Article  Google Scholar 

  4. L. M. Polyanskaya, Gorbacheva M.A., Milanovskii E.Y., and D. G. Zvyagintsev, “Development of microorganisms in the chernozem under aerobic and anaerobic conditions,” Eurasian Soil Sci. 43 (3), 328–332 (2010).

    Article  Google Scholar 

  5. L. M. Polyanskaya and D. G. Zvyagintsev, “The content and composition of microbial biomass as an index of the ecological status of soil,” Eurasian Soil Sci. 38 (6), 625–633 (2005).

    Google Scholar 

  6. N. Kh. Sergaliev, M. G. Kakishev, A.T. Zhiengaliev, M. A. Volodin, E. E. Andronov, and A. G. Pinaev, “Application of a new purification method of West-Kazakhstan chestnut soil microbiota DNA for metagenomic analysis,” Eurasian Soil Sci. 48 (4), 425–431 (2015). doi: doi 10.7868/S0032180X15040103

    Article  Google Scholar 

  7. N. B. Khitrov and S. V. Loiko, “Soil cover patterns on flat interfluves in the Kamennaya Steppe,” Eurasian Soil Sci. 43 (12), 1309–1321 (2010).

    Article  Google Scholar 

  8. A. M. Yaroslavtsev, N. A. Manucharova, A. L. Stepanov, D. G. Zvyagintsev, and I. I. Sudnitsyn, “Microbial destruction of chitin in soils under different moisture conditions,” Eurasian Soil Sci. 42 (7), 797–806 (2009).

    Article  Google Scholar 

  9. R. Amann, W. Ludwig, and K. H. Schleifer, “Phylogenetic identification and in situ detection of individual microbial cells without cultivation,” Microbiol. Rev. 59, 143–169 (1995).

    Google Scholar 

  10. R. I. Amann and W. Ludwig, “Ribosomal RNA targeted nucleic acid probes for studies in microbial ecology,” FEMS Microbiol. Rev. 24, 555–565 (2000).

    Article  Google Scholar 

  11. L. R. Bakken and Å. Frostegård, “Nucleic acid extraction from soil,” in Nucleic Acids and Proteins in Soil, Ed. by P. Nannipieri and K. Smalla (Springer-Verlag, Berlin, 2006), Vol. 8, pp. 49–73.

    Article  Google Scholar 

  12. E. Blume, M. Bischoff, J. Reichert, T. Moorman, A. Konopka, and R. Turco, “Surface and subsurface microbial biomass, community structure and metabolic activity as a function of soil depth and season,” Appl. Soil Ecol. 20 (3), 171–181 (2002).

    Article  Google Scholar 

  13. P. Cao, L. M. Zhang, J. P. Shen, Y. M. Zheng, H. J. Di, and J. Z. He, “Distribution and diversity of archaeal communities in selected Chinese soils,” FEMS Microbiol. Ecol. 80, 146–158 (2012).

    Article  Google Scholar 

  14. H. Daims, A. Brühl, R. Amann, K.-H. Schleifer, and M. Wagner, “The domain-specific probe EUB338 is insufficient for the detection of all bacteria: development and evaluation of a more comprehensive probe set,” Syst. Appl. Microbiol. 22, 434–444 (1999).

    Article  Google Scholar 

  15. T. Eickhorst and R. Tippkotter, “Improved detection of soil microorganisms using fluorescence in situ hybridization (FISH) and catalyzed reporter deposition (CARD-FISH),” Soil Biol. Biochem. 40, 1883–1891 (2008).

    Article  Google Scholar 

  16. K. G. Eilers, C. L. Lauber, R. Knight, and N. Fierer, “Shifts in bacterial community structure associated with inputs of low molecular weight carbon compounds to soil,” Soil Biol. Biochem. 42, 896–903 (2010).

    Article  Google Scholar 

  17. C. M. Hansel, S. Fendorf, P. M. Jardine, and C. A. Francis, “Changes in bacterial and archaeal community structure and functional diversity along a geochemically variable soil profile,” Appl. Environ. Microbiol. 74, 1620–1633 (2008).

    Article  Google Scholar 

  18. M. Hartmann, S. Lee, S. J. Hallam, and W. W. Mohn, “Bacterial, archaeal and eukaryal community structures throughout soil horizons of harvested and naturally disturbed forest stands,” Environ. Microbiol. 11, 3045–3062 (2009).

    Article  Google Scholar 

  19. J.-Z. He, H.-W. Hu, and L.-M. Zhang, “Current insights into the autotrophic thaumarchaeal ammonia oxidation in acidic soils,” Soil Biol. Biochem. 55, 146–154 (2012).

    Article  Google Scholar 

  20. J.-Z. He, J.-P. Shen, L.-M. Zhang, Y.-G. Zhu, Y.-M. Zheng, M.-G. Xu, and H. Di, “Quantitative analyses of the abundance and composition of ammonia-oxidizing bacteria and ammonia-oxidizing archaea of a Chinese upland red soil under long-term fertilization practices,” Environ. Microbiol. 9, 2364–2374 (2007).

    Article  Google Scholar 

  21. Z. J. Jia and R. Conrad, “Bacteria rather than Archaea dominate microbial ammonia oxidation in an agricultural soil,” Environ. Microbiol. 11, 1658–1671 (2009).

    Article  Google Scholar 

  22. R. G. Joergensen and T. Mueller, “The fumigationextraction method to estimate soil microbial biomass: calibration of the kEN value,” Soil Biol. Biochem. 28, 33–37 (1996).

    Article  Google Scholar 

  23. D. Kemnitz, S. Kolb, and R. Conrad, “High abundance of Crenarchaeota in a temperate acidic forest soil,” FEMS Microbiol. Ecol. 60, 442–448 (2007).

    Article  Google Scholar 

  24. S. Leininger, T. Urich, M. Schloter, L. Schwark, J. Qi, and G. W. Nicol, “Archaea predominate among ammonia oxidizing prokaryotes in soils,” Nature 442, 806–809 (2006).

    Article  Google Scholar 

  25. S. Levicnik-Höfferle, G. W. Nicol, L. Pal, J. Hacin, J. I. Prosser, and I. Mandic-Mulec, “Ammonium supply rate influences archaeal and bacterial ammonia oxidizers in a wetland soil vertical profile,” FEMS Microbiol. Ecol. 74, 302–315 (2010).

    Article  Google Scholar 

  26. M. Lupatini, A. K. A. Suleiman, R. J. S. Jacques, Z. I. Antoniolli, E. E. Kuramae, and F. A. D. Camargo, “Soil-borne bacterial structure and diversity does not reflect community activity in Pampa biome,” PLoS One 8 (10), e76465 (2013). doi: 10.1371/journal. pone.0076465

    Article  Google Scholar 

  27. W. Martens-Habbena, P. M. Berube, H. Urakawa, J. R. de la Torre, and D. A. Stahl, “Ammonia oxidation kinetics determine niche separation of nitrifying Archaea and Bacteria,” Nature 461, 976–979 (2009).

    Article  Google Scholar 

  28. A. Mikkonen, M. Santalahti, K. Lappi, A.-M. Pulkkinen, L. Montonen, and L. Suominen, “Bacterial and archaeal communities in long-term contaminated surface and subsurface soil evaluated through coextracted RNA and DNA,” FEMS Microbiol. Ecol. 90 (1), 103–114 (2014).

    Article  Google Scholar 

  29. S. Molin and M. Givskov, “Application of molecular tools for in situ monitoring of bacterial growth activity,” Environ. Microbiol. 1, 383–391 (1999).

    Article  Google Scholar 

  30. G. W. Nicol, S. Leininger, C. Schleper, and J. I. Prosser, “The influence of soil pH on the diversity, abundance, and transcriptional activity of ammonia oxidizing Archaea and Bacteria,” Environ. Microbiol. 10, 2966–2978 (2008).

    Article  Google Scholar 

  31. G. W. Nicol, D. Tscherko, L. Chang, U. Hammesfahr, and J. I. Prosser, “Crenarchaeal community assembly and microdiversity in developing soils at two sites associated with deglaciation,” Environ. Microbiol. 8, 1382–1393 (2006).

    Article  Google Scholar 

  32. G. W. Nicol, G. Webster, L. A. Glover, and J. I. Prosser, “Differential response of archaeal and bacterial communities to nitrogen inputs and pH changes in upland pasture rhizosphere soil,” Environ. Microbiol. 6, 861–867 (2004).

    Article  Google Scholar 

  33. T. Ochsenreiter, D. Selezi, A. Quaiser, L. Bonch-Osmolovskaya, and C. Schleper, “Diversity and abundance of Crenarchaeota in terrestrial habitats studied by 16S RNA surveys and real time PCR,” Environ. Microbiol. 5, 787–797 (2003).

    Article  Google Scholar 

  34. D. Richter and D. Markewitz, “How deep is soil?” Bioscience 45, 600–609 (1995).

    Article  Google Scholar 

  35. J. N. Rooney-Varga, M. W. Giewat, K. N. Duddleston, J. P. Chanton, and M. E. Hines, “Links between archaeal community structure, vegetation type and methanogenic pathway in Alaskan peatlands,” FEMS Microbiol. Ecol. 60, 240–251 (2007).

    Article  Google Scholar 

  36. C. Rumpel and I. Kogel-Knabner, “Deep soil organic matter–a key, but poorly understood component of terrestrial C cycle,” Plant Soil 338, 143–158 (2011).

    Article  Google Scholar 

  37. H. Schmidt and T. Eickhorst, “Detection and quantification of native microbial populations on soil-grown rice roots by catalyzed reporter deposition fluorescence in situ hybridization,” FEMS Microbiol. Ecol. 87, 390–402 (2014).

    Article  Google Scholar 

  38. M. Stursová and P. Baldrian, “Effects of soil properties and management on the activity of soil organic matter transforming enzymes and the quantification of soilbound and free activity,” Plant Soil 338, 99–110 (2011).

    Article  Google Scholar 

  39. D. L. Valentine, “Adaptations to energy stress dictate the ecology and evolution of the Archaea,” Nat. Rev. Microbiol. 5, 316–323 (2007).

    Article  Google Scholar 

  40. E. D. Vance, P. C. Brookes, and D. S. Jenkinson, “An extraction method for measuring soil microbial biomass C,” Soil Biol. Biochem. 19 (6), 703–707 (1987).

    Article  Google Scholar 

  41. C. B. Walker, J. R. de la Torre, M. G. Klotz, H. Urakawa, N. Pinel, and D. J. Arp, “Nitrosopumilus maritimus genome reveals unique mechanisms for nitrification and autotrophy in globally distributed marine Crenarchaea,” Proc. Natl. Acad. Sci. U.S.A. 107, 8818–8823 (2010).

    Article  Google Scholar 

  42. K. Wallenius, H. Rita, A. Mikkonen, K. Lappi, K. Lindström, H. Hortikoinen, A. Raateland, and R. M. Niemi, “Effects of land use on the level, variation and spatial structure of soil enzyme activities and bacterial communities,” Soil Biol. Biochem. 43, 1464–1473 (2011).

    Article  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to M. V. Semenov.

Additional information

Original Russian Text © M.V. Semenov, N.A. Manucharova, A.L. Stepanov, 2016, published in Pochvovedenie, 2016, No. 2, pp. 239–248.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Semenov, M.V., Manucharova, N.A. & Stepanov, A.L. Distribution of Metabolically Active Prokaryotes (Archaea and Bacteria) throughout the Profiles of Chernozem and Brown Semidesert Soil. Eurasian Soil Sc. 49, 217–225 (2016). https://doi.org/10.1134/S1064229316020101

Download citation

  • Received:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S1064229316020101

Keywords

Navigation