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The effect of combined pollution by PAHs and heavy metals on the topsoil microbial communities of Spolic Technosols of the lake Atamanskoe, Southern Russia

Abstract

The contamination with organic and inorganic pollutants changes significantly soil microbial community structure. These shifts indicate anthropogenic pressure and help to discover new possibilities for soil remediation. In this study, the microbial community structure of Spolic Technosols formed at the territory of a former industrial sludge reservoir near the Kamensk-Shakhtinsky (Southern Russia) was studied using a metagenomics approach. The studied soils contain high concentrations of heavy metals (HM) (up to 72,900 mg kg−1) and 16 priority polycyclic aromatic hydrocarbons (PAHs) (up to 6670 mg kg−1). Its microbial communities demonstrate an excellent adaptability level reflected in their complexity and diversity. As shown by the high values of alpha diversity indices (Shannon values up to 10.1, Chao1 values from 1430 to 4273), instead of decreasing quantitatively and qualitatively on the systemic level, microbial communities tend to undergo complex redistribution. Regardless of contamination level, the share of Actinobacteria and Proteobacteria was consistently high and varied from 20 to 50%. Following the results of the Mann–Whitney U test, there were significant changes of less abundant phyla. The abundance of oligotrophic bacteria from Gemmatimonadetes and Verrucomicrobia phyla and autotrophic bacteria (e.g., Nitrospira) decreased due to the high PAH’s level. And abundance of Firmicutes and amoebae-associated bacteria such as TM6 and soil Chlamydia increased in highly contaminated plots. In the Spolic Technosols studied, the influence of factors on the microbial community composition decreased from PAHs concentration to soil characteristics (organic carbon content) and phylum–phylum interactions. The high concentrations of HMs influenced weakly on the microbial community composition.

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The raw/processed data required to reproduce these findings cannot be shared at this time as the data also form part of an ongoing study.

References

  1. Alekseev, I., Zverev, A., & Abakumov, E. (2021). Organic carbon and microbiome in tundra and forest–tundra permafrost soils, southern Yamal, Russia. Polar Research, 40.

  2. Alekseev, I., Zverev, A., & Abakumov, E. (2020). Microbial communities in permafrost soils of Larsemann hills, Eastern Antarctica: Environmental controls and effect of human impact. Microorganisms, 8(8), 1202.

    CAS  Article  Google Scholar 

  3. Amplicon, P. C. R., Clean‐Up, P. C. R., & Index, P. C. R. (2013). 16s metagenomic sequencing library preparation. 1–28.

  4. Andrews, J. H., & Harris, R. F. (1986). R-and K-selection and microbial ecology. Advances in Microbial Ecology, 99–147.

  5. Bates, S. T., Berg-Lyons, D., Caporaso, J. G., Walters, W. A., Knight, R., & Fierer, N. (2011). Examining the global distribution of dominant archaeal populations in soil. ISME Journal, 5(5), 908–917.

    CAS  Article  Google Scholar 

  6. Bauer, T. V., Linnik, V. G., Minkina, T. M., Mandzhieva, S. S., & Nevidomskaya, D. G. (2018). Ecological–geochemical studies of technogenic soils in the flood plain landscapes of the Seversky Donets, Lower Don Basin. Geochemistry International, 56(10), 992–1002.

    CAS  Article  Google Scholar 

  7. Bergmann, G. T., Bates, S. T., Eilers, K. G., Lauber, C. L., Caporaso, J. G., Walters, W. A., et al. (2011). The under-recognized dominance of Verrucomicrobia in soil bacterial communities. Soil Biology and Biochemistry, 43(7), 1450–1455.

    CAS  Article  Google Scholar 

  8. Bourceret, A., Leyval, C., Faure, P., Lorgeoux, C., & Cébron, A. (2018). High PAH degradation and activity of degrading bacteria during alfalfa growth where a contrasted active community developed in comparison to unplanted soil. Environmental Science and Pollution Research, 25(29), 29556–29571.

    CAS  Article  Google Scholar 

  9. Brzeszcz, J., Steliga, T., Kapusta, P., Turkiewicz, A., & Kaszycki, P. (2016). R-strategist versus K-strategist for the application in bioremediation of hydrocarbon-contaminated soils. International Biodeterioration and Biodegradation, 106, 41–52.

    CAS  Article  Google Scholar 

  10. Caporaso, J. G., Kuczynski, J., Stombaugh, J., Bittinger, K., Bushman, F. D., Costello, E. K., et al. (2010). QIIME allows analysis of high-throughput community sequencing data. Nature Methods, 7(5), 335–336.

    CAS  Article  Google Scholar 

  11. Chodak, M., Gołębiewski, M., Morawska-Płoskonka, J., Kuduk, K., & Niklińska, M. (2013). Diversity of microorganisms from forest soils differently polluted with heavy metals. Applied Soil Ecology, 64, 7–14.

    Article  Google Scholar 

  12. Crits-Christoph, A., Robinson, C. K., Barnum, T., Fricke, W. F., Davila, A. F., Jedynak, B., et al. (2013). Colonization patterns of soil microbial communities in the Atacama Desert. Microbiome, 1(1), 1–13.

    Article  Google Scholar 

  13. Davis, M. R., Zhao, F. J., & McGrath, S. P. (2004). Pollution-induced community tolerance of soil microbes in response to a zinc gradient. Environmental Toxicology and Chemistry: An International Journal, 23(11), 2665–2672.

    CAS  Article  Google Scholar 

  14. Delafont, V., Rodier, M. H., Maisonneuve, E., & Cateau, E. (2018). Vermamoeba vermiformis: A free-living amoeba of interest. Microbial Ecology, 76(4), 991–1001.

    Article  Google Scholar 

  15. Delafont, V., Samba-Louaka, A., Bouchon, D., Moulin, L., & Héchard, Y. (2015). Shedding light on microbial dark matter: A TM 6 bacterium as natural endosymbiont of a free-living amoeba. Environmental Microbiology Reports, 7(6), 970–978.

    CAS  Article  Google Scholar 

  16. DeSantis, T. Z., Hugenholtz, P., Larsen, N., Rojas, M., Brodie, E. L., Keller, K., et al. (2006). Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Applied and Environmental Microbiology, 72(7), 5069–5072.

    CAS  Article  Google Scholar 

  17. Directive document 52.10.556–95. Methodical Instructions. Definition of Polluting Substances in Sediments and Suspension. Roshydromet, Moscow (2002) (in Russian).

  18. Dolinšek, J., Lagkouvardos, I., Wanek, W., Wagner, M., & Daims, H. (2013). Interactions of nitrifying bacteria and heterotrophs: Identification of a Micavibrio-like putative predator of Nitrospira spp. Applied and Environmental Microbiology, 79(6), 2027–2037.

    Article  CAS  Google Scholar 

  19. Edgar, R. C., Haas, B. J., Clemente, J. C., Quince, C., & Knight, R. (2011). UCHIME improves sensitivity and speed of chimera detection. Bioinformatics, 27(16), 2194–2200.

    CAS  Article  Google Scholar 

  20. Epelde, L., Lanzén, A., Martín, I., Virgel, S., Mijangos, I., Besga, G., & Garbisu, C. (2019). The microbiota of technosols resembles that of a nearby forest soil three years after their establishment. Chemosphere, 220, 600–610.

    CAS  Article  Google Scholar 

  21. Glazovskaya, M. A. (2012). Geochemical barriers in plain soils: Their typology, functional features, and ecological significance. Vestn. Mosk. Univ., Ser, 5, 8–14.

    Google Scholar 

  22. Gorovtsov, A., Minkina, T. M., Morin, T., Zamulina, I. V., Mandzhieva, S. S., Sushkova, S. N., & Rajput, V. (2019). Ecological evaluation of polymetallic soil quality: The applicability of culture-dependent methods of bacterial communities studying. Journal of Soils and Sediments, 19(8), 3127–3138.

    CAS  Article  Google Scholar 

  23. GOST 12536–79 (1979). Soils. Methods for laboratory determination of granulometric (grain) and micro-aggregate composition.—Introduction. 1980–07–01. Moscow: Standartinform. (In Russian).

  24. Harantová, L., Mudrák, O., Kohout, P., Elhottová, D., Frouz, J., & Baldrian, P. (2017). Development of microbial community during primary succession in areas degraded by mining activities. Land Degradation and Development, 28(8), 2574–2584.

    Article  Google Scholar 

  25. Hill, T. C., Walsh, K. A., Harris, J. A., & Moffett, B. F. (2003). Using ecological diversity measures with bacterial communities. FEMS Microbiology Ecology, 43(1), 1–11.

    CAS  Article  Google Scholar 

  26. Holmes, A. J., Tujula, N. A., Holley, M., Contos, A., James, J. M., Rogers, P., & Gillings, M. R. (2001). Phylogenetic structure of unusual aquatic microbial formations in Nullarbor caves. Australia. Environmental Microbiology, 3(4), 256–264.

    CAS  Article  Google Scholar 

  27. Horn, M., Wagner, M., Müller, K. D., Schmid, E. N., Fritsche, T. R., Schleifer, K. H., & Michel, R. (2000). Neochlamydia hartmannellae gen. nov., sp. Nov.(Parachlamydiaceae), an endoparasite of the amoeba Hartmannella vermiformisThe GenBank accession number for the sequence reported in this paper is AF177275. Microbiology, 146(5), 1231–1239.

    CAS  Article  Google Scholar 

  28. Horn, M. (2008). Chlamydiae as symbionts in eukaryotes. Annual Review of Microbiology, 62, 113–131.

    CAS  Article  Google Scholar 

  29. ISO 10381–1, (2002). Soil quality. Sampling. Part 1. Guidance on the design of sampling programs.

  30. ISO 13859–2014, (2014). Soil Quality. Determination of Polycyclic Aromatic Hydrocarbons (PAH) by Gas Chromatography (GC) and High Performance Liquid Chromatography (HPLC).

  31. ISO 13877–2005, (2005). Soil quality-determination of polynuclear aromatic hydrocarbons—method using high performance liquid chromatography.

  32. Jariwala, S., Redding, L., & Hewitt, D. (2017). The severely under-recognized public health risk of strongyloidiasis in North American cities—A One Health approach. Zoonoses and Public Health. https://doi.org/10.1111/zph.12371

    Article  Google Scholar 

  33. Jiao, S., Zhang, Z., Yang, F., Lin, Y., Chen, W., & Wei, G. (2017). Temporal dynamics of microbial communities in microcosms in response to pollutants. Molecular Ecology, 26(3), 923–936.

    CAS  Article  Google Scholar 

  34. Jost, L., & Banos, T. (2006). Entropy and diversity. Oikos, 113(2), 363–375.

    Article  Google Scholar 

  35. Kandeler, F., Kampichler, C., & Horak, O. (1996). Influence of heavy metals on the functional diversity of soil microbial communities. Biology and Fertility of Soils, 23(3), 299–306.

    CAS  Article  Google Scholar 

  36. Kebbi-Beghdadi, C., & Greub, G. (2014). Importance of amoebae as a tool to isolate amoeba-resisting microorganisms and for their ecology and evolution: The C hlamydia paradigm. Environmental Microbiology Reports, 6(4), 309–324.

    Article  Google Scholar 

  37. Keith, A. M., Schmidt, O., & McMahon, B. J. (2016). Soil stewardship as a nexus between Ecosystem Services and One Health. Ecosystem Services. https://doi.org/10.1016/j.ecoser.2015.11.008

    Article  Google Scholar 

  38. Lauber, C. L., Hamady, M., Knight, R., & Fierer, N. (2009). Pyrosequencing-based assessment of soil pH as a predictor of soil bacterial community structure at the continental scale. Applied and Environmental Microbiology, 75(15), 5111–5120.

    CAS  Article  Google Scholar 

  39. Liu, J., He, X. X., Lin, X. R., Chen, W. C., Zhou, Q. X., Shu, W. S., & Huang, L. N. (2015). Ecological effects of combined pollution associated with e-waste recycling on the composition and diversity of soil microbial communities. Environmental Science and Technology, 49(11), 6438–6447.

    CAS  Article  Google Scholar 

  40. Mackenzie, J. S., & Jeggo, M. (2019). The one health approach-why is it so important? Tropical Medicine and Infectious Disease. https://doi.org/10.3390/tropicalmed4020088

    Article  Google Scholar 

  41. Maila, M. P., Randima, P., Drønen, K., & Cloete, T. E. (2006). Soil microbial communities: Influence of geographic location and hydrocarbon pollutants. Soil Biology and Biochemistry, 38(2), 303–310.

    CAS  Article  Google Scholar 

  42. Minkina, T., Nevidomskaya, D., Bauer, T., Shuvaeva, V., Soldatov, A., Mandzhieva, S., et al. (2018). Determining the speciation of Zn in soils around the sediment ponds of chemical plants by XRD and XAFS spectroscopy and sequential extraction. Science of the Total Environment, 634, 1165–1173.

    CAS  Article  Google Scholar 

  43. Minkina, T., Nevidomskaya, D., Shuvaeva, V., Bauer, T., Soldatov, A., Mandzhieva, S., et al. (2019). Molecular characterization of Zn in Technosols using X-ray absorption spectroscopy. Applied Geochemistry, 104, 168–175.

    CAS  Article  Google Scholar 

  44. Minkina, T., Konstantinova, E., Bauer, T., Mandzhieva, S., Sushkova, S., Chaplygin, V., Burachevskaya, M., Nazarenko, O., Kizilkaya, R., Gülser, C., & Maksimov, A. (2021). Environmental and human health risk assessment of potentially toxic elements in soils around the largest coal-fired power station in Southern Russia. Environmental Geochemistry and Health, 43(6), 2285-2300.

  45. Müller, A. K., Westergaard, K., Christensen, S., & Sørensen, S. J. (2001). The effect of long-term mercury pollution on the soil microbial community. FEMS Microbiology Ecology, 36(1), 11–19.

    Article  Google Scholar 

  46. Perel’man, A. I. (1967). Geochemistry of epigenesis. Plenum Press.

    Book  Google Scholar 

  47. Pires, C., Franco, A. R., Pereira, S. I., Henriques, I., Correia, A., Magan, N., & Castro, P. M. (2017). Metal (loid)-contaminated soils as a source of culturable heterotrophic aerobic bacteria for remediation applications. Geomicrobiology Journal, 34(9), 760–768.

    CAS  Article  Google Scholar 

  48. Procedure of measurements benz(a)pyrene content in soils, sediments and sludges by highly effective liquid chromatography method (2008). Certificate 27–08: Moscow. 27p. (in Russian).

  49. Rudnick, R. L., Gao, S., Holland, H. D., & Turekian, K. K. (2003). Composition of the continental crust. The Crust, 3, 1–64.

    Google Scholar 

  50. Santos, E. S., Abreu, M. M., Macías, F., & de Varennes, A. (2016). Chemical quality of leachates and enzymatic activities in Technosols with gossan and sulfide wastes from the São Domingos mine. Journal of Soils and Sediments, 16(4), 1366–1382.

    CAS  Article  Google Scholar 

  51. Schloss, P. D., Westcott, S. L., Ryabin, T., Hall, J. R., Hartmann, M., Hollister, E. B., et al. (2009). Introducing mothur: Open-source, platform-independent, community-supported software for describing and comparing microbial communities. Applied and Environmental Microbiology, 75(23), 7537–7541.

    CAS  Article  Google Scholar 

  52. Schneider, A. R., Gommeaux, M., Duclercq, J., Fanin, N., Conreux, A., Alahmad, A., & Marin, B. (2017). Response of bacterial communities to Pb smelter pollution in contrasting soils. Science of the Total Environment, 605, 436–444.

    Article  CAS  Google Scholar 

  53. Shi, Y., Queller, D. C., Tian, Y., Zhang, S., Yan, Q., He, Z., et al. (2020). The Ecology and Evolution of Amoeba-Bacterium Interactions. Applied and Environmental Microbiology, 87(2), e0186620.

    Google Scholar 

  54. Šimonovičová, A., Ferianc, P., Vojtková, H., Pangallo, D., Hanajík, P., Kraková, L., et al. (2017). Alkaline technosol contaminated by former mining activity and its culturable autochthonous microbiota. Chemosphere, 171, 89–96.

    Article  CAS  Google Scholar 

  55. Stefanowicz, A. M., Kapusta, P., Zubek, S., Stanek, M., & Woch, M. W. (2020). Soil organic matter prevails over heavy metal pollution and vegetation as a factor shaping soil microbial communities at historical Zn–Pb mining sites. Chemosphere, 240, 124922.

    CAS  Article  Google Scholar 

  56. Sushkova, S. N., Minkina, T. M., Turina, I. G., Mandzhieva, S. S., Bauer, T. V., Kizilkaya, R., & Zamulina, I. V. (2017). Monitoring of benzo[a]pyrene content in soils under the effect of long-term technogenic pollution. Journal of Geochemical Exploration, 174, 100–106.

    CAS  Article  Google Scholar 

  57. Sushkova, S., Minkina, T., Tarigholizadeh, S., Antonenko, E., Konstantinova E., Gülser, C., Dudnikova, T., Barbashev, A., & Kizilkaya R. (2020). PAHs accumulation in soil-plant system of Phragmites australis Cav. in soil under long-term chemical contamination. Eurasian Journal of Soil Science (EJSS), 9(3), 242–253.

  58. Sushkova, S., Minkina, T., Tarigholizadeh, S., Rajput, V., Fedorenko, A., Antonenko, E., Dudnikova, T., Chernikova, N., Yadav, B.K., & Batukaev, A. (2021). Soil PAHs contamination effect on the cellular and subcellular organelle changes of Phragmites australis Cav. Environmental Geochemistry and Health, 43(6), 2407–2421.

  59. Thompson, I. P., Bailey, M. J., Ellis, R. J., Maguire, N., & Meharg, A. A. (1998). Response of soil microbial communities to single and multiple doses of an organic pollutant. Soil Biology and Biochemistry, 31(1), 95–105.

    Article  Google Scholar 

  60. Tripathi, B. M., Kim, M., Singh, D., Lee-Cruz, L., Lai-Hoe, A., Ainuddin, A. N., & Adams, J. M. (2012). Tropical soil bacterial communities in Malaysia: PH dominates in the equatorial tropics too. Microbial Ecology, 64(2), 474–484.

    Article  Google Scholar 

  61. Uzarowicz, Ł, Wolińska, A., Błońska, E., Szafranek-Nakonieczna, A., Kuźniar, A., Słodczyk, Z., & Kwasowski, W. (2020). Technogenic soils (Technosols) developed from mine spoils containing Fe sulphides: Microbiological activity as an indicator of soil development following land reclamation. Applied Soil Ecology, 156, 103699.

    Article  Google Scholar 

  62. Vinogradov, A. P. (1957). Geochemistry of rare and trace elements in soils. RAN.

    Google Scholar 

  63. Viti, C., Mini, A., Ranalli, G., Lustrato, G., & Giovannetti, L. (2006). Response of microbial communities to different doses of chromate in soil microcosms. Applied Soil Ecology, 34(2–3), 125–139.

    Article  Google Scholar 

  64. Winding, A., Modrzyński, J. J., Christensen, J. H., Brandt, K. K., & Mayer, P. (2019). Soil bacteria and protists show different sensitivity to polycyclic aromatic hydrocarbons at controlled chemical activity. FEMS Microbiology Letters, 366(17), fnz214.

    CAS  Article  Google Scholar 

  65. Wolińska, A., Gałązka, A., Kuźniar, A., Goraj, W., Jastrzębska, N., Grządziel, J., & Stępniewska, Z. (2018). Catabolic fingerprinting and diversity of bacteria in mollic gleysol contaminated with petroleum substances. Applied Sciences, 8(10), 1970.

    Article  CAS  Google Scholar 

  66. Xu, X., Zhang, Z., Hu, S., Ruan, Z., Jiang, J., Chen, C., & Shen, Z. (2017). Response of soil bacterial communities to lead and zinc pollution revealed by Illumina MiSeq sequencing investigation. Environmental Science and Pollution Research, 24(1), 666–675.

    Article  CAS  Google Scholar 

  67. Yeoh, Y. K., Sekiguchi, Y., Parks, D. H., & Hugenholtz, P. (2016). Comparative genomics of candidate phylum TM6 suggests that parasitism is widespread and ancestral in this lineage. Molecular Biology and Evolution, 33(4), 915–927.

    CAS  Article  Google Scholar 

  68. Zhou, Y., Hartemink, A. E., Shi, Z., Liang, Z., & Lu, Y. (2019). Land use and climate change effects on soil organic carbon in North and Northeast China. Science of the Total Environment, 647, 1230–1238.

    CAS  Article  Google Scholar 

  69. Zornoza, R., Acosta, J. A., Faz, A., & Bååth, E. (2016). Microbial growth and community structure in acid mine soils after addition of different amendments for soil reclamation. Geoderma, 272, 64–72.

    CAS  Article  Google Scholar 

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Acknowledgements

The present research was funded by the Russian Science Foundation through Project No. 19-74-10046. We thank the centers for collective use of Southern Federal University "Modern Microscopy" and "High Technology" for performing chemical-analytical experiments and center for collective use of Kazan Federal University "Interdisciplinary Center of Shared Facilities" for performing metagenomics analysis.

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AG contributed to conceptualization, formulation of a research problem, and writing. KD contributed to data processing, methodology, discussion, and writing. TM contributed to data curation and writing—reviewing. SS contributed to writing, analytical work, HPLC, and data performing. TG conducted experiments. TD contributed to visualization and statistical processing, and methodology. AB conducted experiments and contributed to data creating and experiments design. IS contributed to writing—review and editing. VR contributed to bioinformatics, experiment design, writing—review, and editing. AL contributed to DNA extraction and bioinformatics. VR contributed to data processing. YK contributed to writing—review and editing.

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Correspondence to Svetlana Sushkova.

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Gorovtsov, A., Demin, K., Sushkova, S. et al. The effect of combined pollution by PAHs and heavy metals on the topsoil microbial communities of Spolic Technosols of the lake Atamanskoe, Southern Russia. Environ Geochem Health (2021). https://doi.org/10.1007/s10653-021-01059-x

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Keywords

  • Anthropogenic impact
  • Restoration
  • Toxic elements
  • Soil pollution
  • Metagenomics
  • Heavy metals
  • PAH's
  • Microbial communities
  • Long-term contamination