Skip to main content
SpringerLink
Log in

Changes in the Phylogenetic Structure of the Metabolically Active Prokaryotic Soil Complex Induced by Oil Pollution

  • EXPERIMENTAL ARTICLES
  • Published:
Microbiology Aims and scope Submit manuscript

Abstract—

Molecular genetic techniques (FISH and metabarcoding) were used to investigate comparative biodiversity in the prokaryotic complex of soil microcosms of gray forest, chestnut, and chernozem soils before and after oil pollution. At the level of high-rank taxonomic units, the structure of prokaryotic communities from different soil types was similar. In oil-polluted microcosms microbial diversity decreased, and the metbolically active dominants of the Bacteria and Archaea domains changed compared to the control samples. A specific bacterial complex was found to emerge in experimental samples of all soil types, with predominance of the Gammaproteobacteria and Actinobacteria, as well as of archaea, among which Thaumarchaeota and Crenarchaeota prevailed. Members of the soil prokaryotic complex active and inactive in respect to oil pollution were determined. Our results indicate similar succession responses of microbial communities from different soil type to oil pollution.

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.
Fig. 3.
Fig. 4.
Fig. 5.
Fig. 6.
Fig. 7.
Fig. 8.

Similar content being viewed by others

REFERENCES

  1. Amann, R.I., Krunholz, L., and Stahl, D.A., Fluorescent-oligonucleotide probing of whole cells for determinative, phylogenetic and environmental studies in microbiology, J. Bacteriol., 1990, vol. 172, pp. 762–770.

    Article  CAS  Google Scholar 

  2. Efimenko, T.A., Malanicheva, I.A., Vasil’eva, B.F., Glukhova, A.A., Sumarukova, I.G., Boikova, Yu.V., Mal-kina, N.D., Terekhova, L.P., and Efremenkova, O.V., Antibiotic activity of bacterial endobionts of basidiomycete fruit bodies, Microbiology (Moscow), 2016, vol. 85, pp. 752–758.

    Article  CAS  Google Scholar 

  3. Filonov, A.E., Akhmetov, L.I., Puntus, I.F., Esikova, T.Z., Gafarov, A.B., Kosheleva, I.A., and Boronin, A.M., Horizontal transfer of catabolic plasmids and naphthalene biodegradation in open soil, Microbiology (Moscow), 2010, vol. 79, pp. 184–190.

    Article  CAS  Google Scholar 

  4. Gennadiev, A.N., Pikovskii, Y.I., Zhidkin, A.P., Kovach, R.G., Koshovskii, T.S., Smirnova, M.A., Khly-nina, N.I., and Tsibart, A.S., Factors and features of the hydrocarbon status of soils, Euras. Soil Sci., 2015, vol. 48, pp. 1193–1206.

    Article  CAS  Google Scholar 

  5. Guzev, V.S., Bondarenko, N.G., and Byzov, B.A., The structure of the initiated microbial community as an integral method for assessing the microbiological state of soils, Microbiology (Moscow), 1980, vol. 49, pp. 134–139.

    CAS  PubMed  Google Scholar 

  6. Itoh, T., Yamanoi, K., Kudo, T., Ohkuma, M., and Takashina, T., Aciditerrimonas ferrireducens gen. nov., sp. nov., an iron-reducing thermoacidophilic actinobacterium isolated from a solfataric field, Int. J. Syst. Evol. Microbiol., 2011, vol. 61, pp. 1281–1285.

    Article  Google Scholar 

  7. IUSS Working Group WRB, World Reference Base for Soil Resources 2014: International soil classification system for naming soils and creating legends for soil maps, World Soil Resources Reports no. 106, Rome: FAO, 2014.

  8. Ivanova, A.A., Vetrova, A.A., Filonov, A.E., and Boro-nin, A.M., Oil biodegradation by microbial–plant associations, Appl. Biochem. Microbiol., 2015, vol. 51, pp. 196–201.

    Article  CAS  Google Scholar 

  9. Ivshina, I.B., Kostina, L.V., Kamenskikh, T.N., Zhuikova, V.A., Zhuikova, T.V., and Bezel’, V.S., Soil microbiocenosis as an indicator of stability of meadow communities in the environment polluted with heavy metals, Russ. J. Ecol., 2014, vol. 45, pp. 83–89.

    Article  CAS  Google Scholar 

  10. Ivshina, I.B., Kuzyukina, M.S., and Krovoruchko, A.V., Immobilization of hydrocarbon-oxidizing rhodococci as a factor accelerating oil remediation, in Immobilizatsiya kletok: Biokatalizatory i protsessy (Cell Immobilization: Biocatalysts and Processes), Efremenko, E.N., Ed., Moscow: RIOR, 2018, pp. 405–424.

  11. Juretschko, S., Loy, A., Lehner, A., and Wagner, M., The microbial community composition of a nitrifying-denitrifying activated sludge from an industrial sewage treatment plant analyzed by the full-cycle rRNA approach, Syst. Appl. Microbiol., 2002, vol. 25, pp. 84–99.

    Article  CAS  Google Scholar 

  12. Klassifikatsiya i diagnostika pochv SSSR (Classification and Diagnostics of Soils in the USSR), Moscow: Kolos, 1977.

  13. Lysak, L.V. and Dobrovolskaya, T.G., Bacteria in tundra soils of Western Taimyr, Soviet Soil Sci., 1982, no. 9, pp. 74–78.

  14. Manucharova, N.A., Kol’tsova, E.M., Stepanov, A.L., Demkina, E.V., Demkin, V.A., and El’Registan G.I., Comparative analysis of the functional activity and composition of hydrolytic microbial complexes from the lower Volga barrow and modern chestnut soils, Microbiology (Moscow), 2014, vol. 83, pp. 674–683.

    Article  CAS  Google Scholar 

  15. Manucharova, N.A., Kuteinikova, Yu.V., Ivanov, P.V., Nikolaeva, S.K., Trofimov, V.T., Stepanov, P.Yu, Tyapkina, E.V., Lipatov, D.N., and Stepanov, A.L., Molecular analysis of the hydrolytic component of petroleum contaminated soils and of soils remediated with chitin, Microbiology (Moscow), vol. 86, pp. 395–402.

  16. Manz, W., Amann, R., Ludwig, W., Vancanneyt, M., and Schleifer, K.-H., Application of a suite of 16S rRNA-specific oligonucleotide probes designed to investigate bacteria of the phylum Cytophaga-Flavobacter-Bacteroides in the natural environment, Microbiology (SGM), 1996, vol. 142, pp. 1097–1106.

    Article  CAS  Google Scholar 

  17. Manz, W., Amann, R., Ludwig, W., Wagner, M., and Schleifer, K.-H., Phylogenetic oligonucleotide probes for the major subclasses of Proteobacteria: problems and solutions, Syst. Appl. Microbiol., 1992, vol. 15, pp. 593–600.

    Article  Google Scholar 

  18. Meier, H., Amann, R., Ludwig, W., and Schleifer, K.-H., Specific oligonucleotide probes for in situ detection of a major group of gram-positive bacteria with low DNA G + C content, Syst. Appl. Microbiol., 1999, vol. 22, pp. 186–196.

    Article  CAS  Google Scholar 

  19. Monciardini, P., Sosio, M., Cavaletti, L., Chiocchini, C., and Donadio, S., New PCR primers for the selective amplification of 16S rDNA from different groups of actinomycetes, FEMS Microbiol. Ecol., 2002, vol. 42, pp. 419–429.

    CAS  PubMed  Google Scholar 

  20. Nazina, T.N., Shestakova, N.M., Grigor’yan, A.A., Mikhailova, E.M., Tourova, T.P., Belyaev, S.S., Poltaraus, A.B., Feng, C., and Ni, F., Phylogenetic diversity and activity of anaerobic microorganisms of high-temperature horizons of the Dagang oil field (P.R. China), Microbiology (Moscow), 2006, vol. 75, pp. 55–65.

    Article  CAS  Google Scholar 

  21. Nazina, T.N., Sokolova, D.S., Babich, T.L., Semenova, E.M., Ershov, A.P., Bidzhieva, S.K., Borzenkov, I.A., Tourova, T.P., Poltaraus, A.B., and Khisametdinov, M.R., Microorganisms of low-temperature heavy oil reservoirs (Russia) and their possible application for enhanced oil recovery, Microbiology (Moscow), 2017, vol. 86, pp. 773–785.

    Article  CAS  Google Scholar 

  22. Nazina, T.N., Tourova, T.P., Poltaraus, A.B., Novikova, E.V., Grigoriyan, A.A., Ivanova, A.E., Petru-nyaka, V.V., Osipov, G.A., Belyaev, S.S., and Ivanov, M.V., Taxonomic study of aerobic thermophilic bacilli: descriptions of Geobacillus subterraneus gen. nov., sp. nov. and Geobacillus uzenensis sp. nov. from petroleum reservoirs and transfer of Bacillus stearothermophilus, Bacillus thermocatenulatus, Bacillus thermooleovorans, Bacillus kaustophilus, Bacillus thermoglucosidasius and Bacillus thermodenitrificans to Geobacillus as the new combinations G. stearothermophilus, G. thermocatenulatus, G. thermoleovorans, G. kaustophilus, G. thermoglucosidasius and G. thermodenitrificans,Int. J. Syst. Evol. Microbiol., 2001, vol. 51, pp. 433–446.

    Article  CAS  Google Scholar 

  23. Neef, A., Amann, R., Schlesner, H., and Schleifer, K.-H., Monitoring a widespread bacterial group: in situ detection of Planctomycetes with 16S rRNA-targeted probes, Microbiology (SGM), 1998, vol. 144, pp. 3257–3266.

    Article  CAS  Google Scholar 

  24. Polyanskaya, L.M., Geydenbreht, V.V., Stepanov, A.L., and Zvyagintsev, D.G., Distribution of the number and biomass of microorganisms on the profiles of zonal soil types, Euras. Soil Sci., 1995, vol. 27, no. 2, pp. 322–328.

    Google Scholar 

  25. Rabus, R., Wilkes, H., Schramm, A., Harms, G., Behrends, A., Amann, R., and Widdel, F., Anaerobic utilization of alkylbenzenes and n-alkanes from crude oil in an enrichment culture of denitrifying bacteria affiliating with the beta-subclass of Proteobacteria,Environ. Microbiol., 1999, vol. 1, pp. 145–157.

    Article  CAS  Google Scholar 

  26. Roller, C., Wagner, M., Amann, R., Ludwig, W., and Schleifer, K.-H., In situ probing of Gram-positive bacteria with high DNA G + C content using 23S rRNA-targeted oligonucleotides, Microbiology (SGM), 1994, vol. 140, pp. 2849–2858.

    Article  CAS  Google Scholar 

  27. Sharkova, S.Yu., Polyanskova, E.A., and Parfenova, E.A., State of the soil microbial complex under oil contamination, Izv. Penz. Gos. Ped. Univ., 2011, no. 25, pp. 614–617.

  28. Shishov, L.L., Tonkonogov, V.D., Lebedeva, I.I., and Gerasimova, M.I., Klassifikatsiya i diagnostika pochv Rossii (Classification and Diagnostics of Russian Soils), Smolensk: Oikumena, 2004.

  29. Somanadhan, B., Kotturi, S.R., Yan Leong, C., Glover, R.P., Huang, Y., Flotow, H., Buss, A.D., Lear, M.J., and Butler, M.S., Isolation and synthesis of falcitidin, a novel myxobacterial-derived acyltetrapeptide with activity against the malaria target falcipain-2, J. Antibiot. (Tokyo), 2013, vol. 66, pp. 259–264.

    Article  CAS  Google Scholar 

  30. Sorkhoh, N.A., Ghannoum, M.A., Ibrahim, A.S., Stretton, R.J., and Rdaman, S.S., Crude oil and hydrocarbon degrading strains of Rhodococcus: Rhodococcus strains isolated from soil and marine environments in Kuwait, Environ. Pollut., 1990, vol. 65, pp. 1–18.

    Article  CAS  Google Scholar 

  31. Stahl, D.A. and Amann, R., Development and application of nucleic acid probes, in Nucleic Acid Techniques in Bacterial Systematics, Stackebrandt, E. and Goodfellow, M., Eds., N.Y.: Wiley, 1991, pp. 205–248.

    Google Scholar 

  32. Teira, E., Reinthaler, T., Peinthaler, A. Peinthaler, J., and Herndl, G.J., Combining catalyzed reporter deposition-fluorescence in situ hybridization and microautoradiography to detect substrate utilization by Bacteria and Archaea in the deep ocean, Appl. Environ. Microbiol., 2004, vol. 70, pp. 4411–4414.

    Article  CAS  Google Scholar 

  33. Timonen, S. and Bomberg, M., Archaea in dry soil environments, Phytochem. Rev., 2009, vol. 8, pp. 505–518.

    Article  CAS  Google Scholar 

  34. Tolpeshta, I.I., Trofimov, S.Ya., Erkenova, M.I., Sokolova, T.A., Stepanov, A.L., and Lobanenkov, A.M., Laboratory simulation of the successive aerobic and anaerobic degradation of oil products in oil contaminated high moor peat, Euras. Soil Sci., 2015, vol. 48, no. 3, pp. 314–324.

    Article  CAS  Google Scholar 

  35. Trofimov, S.Ya. and Rozanova, M.S., Oil-contamination-induced changes in soil properties, in Degradatsia i okhrana pochv (Soil Degradation and Preservation), Dobrovol’skii, G.V., Ed., Moscow: Nauka, 2002, pp. 359–373.

  36. Uzkikh, O.S. and Khomyakov, D.M., Diagnostics of oil-contaminated soils, Ekol. Normy. Pravila. Informatsiya, 2009, no. 3, pp. 30–36.

  37. Vetrova, A.A., Nechaeva, I.A., Ignatova, A.A., Puntus, I.F., Arinbasarov, M.U., Filonov, A.E., and Boronin, A.M., Effect of catabolic plasmids on physiological parameters and efficiency of oil destruction by Pseudomonas bacteria, Microbiology (Moscow), 2007, vol. 76, pp. 310–316.

    Article  CAS  Google Scholar 

  38. Wagner, M. and Horn, M., The Planctomycetes, Verrucomicrobia, Chlamydiae and sister phyla comprise a superphylum with biotechnological and medical relevance, Curr. Opin. Biotechnol., 2006, vol. 17, pp. 241–249.

    Article  CAS  Google Scholar 

  39. Zvyagintsev, D.G., Ekologiya aktinomitsetov (Ecology of Actinomycetes), Moscow: GEOS, 2001.

  40. Zvyagintsev, D.G., Umarov, M.M., and Chernov, I.Yu., Microbial communities and their functioning in the processes of soil degradation and self-restoration, in Degradatsia i okhrana pochv (Soil Degradation and Preservation), Dobrovol’skii, G.V., Ed., Moscow: Nauka, 2002, pp. 404–454.

Download references

Funding

The work was supported by the Russian Foundation for Basic Research, project no. 19-29-05197-mk.

Author information

Authors and Affiliations

  1. Moscow State University, 119192, Moscow, Russia

    N. A. Manucharova, N. A. Ksenofontova, T. D. Karimov, A. P. Vlasova, G. M. Zenova & A. L. Stepanov

Authors
  1. N. A. Manucharova
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. N. A. Ksenofontova
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. T. D. Karimov
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. A. P. Vlasova
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. G. M. Zenova
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. A. L. Stepanov
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to N. A. Manucharova.

Ethics declarations

The authors declare that they have no conflict of interest. This article does not contain any studies involving animals or human participants performed by any of the authors.

Additional information

Translated by E. Makeeva

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Manucharova, N.A., Ksenofontova, N.A., Karimov, T.D. et al. Changes in the Phylogenetic Structure of the Metabolically Active Prokaryotic Soil Complex Induced by Oil Pollution. Microbiology 89, 219–230 (2020). https://doi.org/10.1134/S0026261720020083

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S0026261720020083

Keywords:

Search

Navigation