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Structure and Seasonal Variability of Microbial Communities of Groundwater in the City of Moscow

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Abstract

Groundwater, which appears on the surface in the form of springs, is an important ecologically significant component of the aquatic ecosystem, sensitive to changes in environmental conditions. The anthropogenic impact associated with urbanization leads to a change in the characteristics of groundwater, which, in turn, affects the composition of microbial communities in spring waters. Using high-throughput sequencing of the 16S ribosomal RNA gene fragments, we characterized the composition of microbial communities in five natural springs in the city of Moscow in the spring, summer, and winter seasons. The microbial communities of each spring in different seasons were similar to each other and clearly differed from the microbiomes of the other springs. Among the Archaea, which averaged about 20% of the microbial communities, ammonium-oxidizing Crenarchaeota predominated, as well as Nanoarchaeota. Most of the Bacteria belonged to the phyla Proteobacteria, Patescibacteria, Verrucomicrobiota, Chloroflexi, and Bacteroidota. Autotrophic bacteria, including iron-oxidizing bacteria of the family Gallionellaceae and nitrifiers, as well as methanotrophs, accounted for significant proportions in the microbial communities of the springs with a presumably deeper water source. Chemical and molecular analyses did not reveal contamination of spring waters with toxic substances and oil-derived products, as well as the presence of pathogenic microorganisms and indicators of fecal pollution. However, during the spring season, the proportions of halophilic and hydrocarbon-oxidizing bacteria increased in water microbiomes, which may reflect the entry into groundwater after snow thawing of deicing reagents and hydrocarbons, which are successfully biodegraded in the soil.

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REFERENCES

  1. Akbari, A., David, C., Rahim, A.A., and Ghoshal, S., Salt selected for hydrocarbon-degrading bacteria and enhanced hydrocarbon biodegradation in slurry bioreactors, Water. Res., 2021, vol. 202, p. 117424.

    Article  CAS  PubMed  Google Scholar 

  2. Bärenstrauch, M., Vanhove, A.S., Allégra, S., Peuble, S., Gallice, F., Paran, F., Lavastre, V., and Girardot, F., Microbial diversity and geochemistry of groundwater impacted by steel slag leachates, Sci. Total. Environ., 2022, vol. 843, pp. 156987.

    Article  PubMed  Google Scholar 

  3. Beam, J.P., Becraft, E.D., Brown, J.M., Schulz, F., Jarett, J.K., Bezuidt, O., Poulton, N., Clark, K., Dunfield, P., Ravin, N., Spear, J., Hedlund, B., Kormas, K., Sievert, S., Elshahed, M., et al., Ancestral absence of electron transport chains in Patescibacteria and DPANN, Front. Microbiol., 2020, vol. 11, p. 1848.

    Article  PubMed  PubMed Central  Google Scholar 

  4. Brown, C.T., Hug, L.A., Thomas, B.C., Sharon, I., Castelle, C.J., Singh, A., Wilkins, M., Wrighton, K., Williams, K., and Banfield, J.F., Unusual biology across a group comprising more than 15% of domain Bacteria, Nature, 2015, vol. 523, pp. 208‒211.

    Article  CAS  PubMed  Google Scholar 

  5. Cao, H., Auguet, J.C., and Gu, J.D., Global ecological pattern of ammonia-oxidizing archaea, PLoS One, 2013, vol. 8, p. e52853.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Chistoserdova, L., Methylotrophy in a lake: from metagenomics to single-organism physiology, Appl. Environ. Microbiol., 2011, vol. 77, pp. 4705‒4711.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. David, G.M., López-García, P., Moreira, D., Alric, B., Deschamps, P., Bertolino, P., Restoux, G., Rochelle-Newall, E., Thébault, E., Simon, M., and Jardillier, L., Small freshwater ecosystems with dissimilar microbial communities exhibit similar temporal patterns, Mol. Ecol., 2021, vol. 30, pp. 2162‒2177.

    Article  CAS  PubMed  Google Scholar 

  8. Dombrowski, N., Lee, J.H., Williams, T.A., Offre, P., and Spang, A., Genomic diversity, lifestyles and evolutionary origins of DPANN archaea, FEMS Microbiol. Lett., 2019, vol. 366, p. fnz008.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Edgar, R.C., Search and clustering orders of magnitude faster than BLAST, Bioinformatics, 2010, vol. 26, pp. 2460–2461.

    Article  CAS  PubMed  Google Scholar 

  10. Emerson, D., Fleming, E.J., and McBeth, J.M., Iron-oxidizing bacteria: an environmental and genomic perspective, Annu. Rev. Microbiol., 2010, vol. 64, pp. 561‒583.

    Article  CAS  PubMed  Google Scholar 

  11. Emerson, D., Field, E.K., Chertkov, O., Davenport, K.W., Goodwin, L., Munk, C., Nolan, M., and Woyke, T., Comparative genomics of freshwater Fe-oxidizing bacteria: implications for physiology, ecology, and systematics, Front. Microbiol., 2013, vol. 4, p. 254.

    Article  PubMed  PubMed Central  Google Scholar 

  12. Ettwig, K.F., Butler, M.K., Le Paslier, D., Pelletier, E., Mangenot, S., Kuypers, M.M., Schreiber, F., Dutilh, B.E., Zedelius, J., de Beer, D., Gloerich, J., Wessels, H.J.C.T., van Alen, T., Luesken, F., Wu, M.L., et al., Nitrite-driven anaerobic methane oxidation by oxygenic bacteria, Nature, 2010, vol. 464, pp. 543‒548.

    Article  CAS  PubMed  Google Scholar 

  13. Fakhrzadegan, I., Hassanshahian, M., Askari Hesni, M., and Saadatfar, A., A study of crude oil-degrading bacteria from mangrove forests in the Persian Gulf, Mar. Ecol., 2019, vol. 40, p. e12544.

    Article  Google Scholar 

  14. Finneran, K.T., Johnsen, C.V., and Lovley, D.R., Rhodoferax ferrireducens sp. nov., a psychrotolerant, facultatively anaerobic bacterium that oxidizes acetate with the reduction of Fe(III), Int. J. Syst. Evol. Microbiol., 2003, vol. 53, pp. 669‒673.

    Article  CAS  PubMed  Google Scholar 

  15. Frey, B., Rime, T., Phillips, M., Stierli, B., Hajdas, I., Widmer, F., and Hartmann, M., Microbial diversity in European alpine permafrost and active layers, FEMS Microbiol. Ecol., 2016, vol. 92, p. fiw018.

    Article  PubMed  Google Scholar 

  16. Govarthanan, M., Khalifa, A.Y., Kamala-Kannan, S., Srinivasan, P., Selvankumar, T., Selvam, K., and Kim, W., Significance of allochthonous brackish water Halomonas sp. on biodegradation of low and high molecular weight polycyclic aromatic hydrocarbons, Chemosphere, 2020, vol. 243, p. 125389.

    Article  CAS  PubMed  Google Scholar 

  17. Grimm, N.B., Foster, D., Groffman, P., Grove, J.M., Hopkinson, C.S., Nadelhoffer, K.J., Pataki, D.E., and Peters, D.P., The changing landscape: ecosystem responses to urbanization and pollution across climatic and societal gradients, Front. Ecol. Environ., 2008, vol. 6, pp. 264‒272.

    Article  Google Scholar 

  18. Harayama, S., Kasai, Y., and Hara, A., Microbial communities in oil-contaminated seawater, Curr. Opin. Biotechnol., 2004, vol. 15, pp. 205‒214.

    Article  CAS  PubMed  Google Scholar 

  19. Haroon, M.F., Hu, S., Shi, Y., Imelfort, M., Keller, J., Hugenholtz, P., Yuan, Z., and Tyson, G.W., Anaerobic oxidation of methane coupled to nitrate reduction in a novel archaeal lineage, Nature, 2013, vol. 500, pp. 567‒570.

    Article  CAS  PubMed  Google Scholar 

  20. Herrmann, M., Wegner, C.E., Taubert, M., Geesink, P., Lehmann, K., Yan, L., Lehmann, R., Totsche, K.U., and Küsel, K., Predominance of Cand. Patescibacteria in groundwater is caused by their preferential mobilization from soils and flourishing under oligotrophic conditions, Front. Microbiol., 2019, vol. 10, p. 1407.

    Article  PubMed  PubMed Central  Google Scholar 

  21. Huang, G., Liu, C., Zhang, Y., and Chen, Z., Groundwater is important for the geochemical cycling of phosphorus in rapidly urbanized areas: a case study in the Pearl River Delta, Environ. Pollut., 2020, vol. 260, p. 114079.

    Article  CAS  PubMed  Google Scholar 

  22. Huu, N.B., Nga, V.H., and Ha, D.T.C., Survey of the petroleum hydrocarbon-degrading capacity of three bacteria strains isolated from the oil sludge in Vietnam, Academia J. Biol., 2003, vol. 25, no. 4, pp. 62‒68.

    Google Scholar 

  23. Il’inskii, V.V., Shadrina, N.A., and Komarova, T.I., Heterotrophic bacteria of urban springs: Krylatskie Kholmy Nature Reserve, Moscow, Water Resour., 2010, vol. 37, pp. 494‒501.

    Article  Google Scholar 

  24. Ivanova, A.A., Oshkin, I.Y., Danilova, O.V., Philippov, D.A., Ravin, N.V., and Dedysh, S.N., Rokubacteria in northern peatlands: habitat preferences and diversity patterns, Microorganisms, 2021, vol. 10, p. 11.

    Article  PubMed  PubMed Central  Google Scholar 

  25. Kato, S., Krepski, S., Chan, C., Itoh, T., and Ohkuma, M., Ferriphaselus amnicola gen. nov., sp. nov., a neutrophilic, stalk-forming, iron-oxidizing bacterium isolated from an iron-rich groundwater seep, Int. J. Syst. Evol. Microbiol., 2014, vol. 64, pp. 921‒925.

    Article  CAS  PubMed  Google Scholar 

  26. Kato, S., Ohkuma, M., Powell, D.H., Krepski, S.T., Oshima, K., Hattori, M., Shapiro, N., Woyke, T., and Chan, C.S., Comparative genomic insights into ecophysiology of neutrophilic, microaerophilic iron oxidizing bacteria, Front. Microbiol., 2015, vol. 6, p. 1265.

    Article  PubMed  PubMed Central  Google Scholar 

  27. Kløve, B., Allan, A., Bertrand, G., Druzynska, E., Ertürk, A., Goldscheider, N., Henry, S., Karakaya, N., Karjalainen, T.P., Koundouri, P., Kupfersberger, H., Kvœrner, J., Lundberg, A., Muotka, T., Preda, E., et al., Groundwater dependent ecosystems. Part II. Ecosystem services and management in Europe under risk of climate change and land use intensification, Environ. Sci. Policy, 2011, vol. 14, pp. 782‒793.

    Article  Google Scholar 

  28. Kolinko, S., Richter, M., Glöckner, F.O., Brachmann, A., and Schüler, D., Single-cell genomics of uncultivated deep-branching magnetotactic bacteria reveals a conserved set of magnetosome genes, Environ. Microbiol., 2016, vol. 18, pp. 21‒37.

    Article  CAS  PubMed  Google Scholar 

  29. Kuroda, K. and Fukushi, T., Groundwater contamination in urban areas, in Groundwater Management in Asian Cities, Takizawa, S., Ed., Tokyo: Springer, 2008, vol. 2, p. 125‒149.

    Google Scholar 

  30. Kuroda, K., Yamamoto, K., Nakai, R., Hirakata, Y., Kubota, K., Nobu, M.K., and Narihiro, T., Symbiosis between Candidatus Patescibacteria and Archaea discovered in wastewater-treating bioreactors, mBio, 2022, p. e01711-22.

  31. Lerner, D.N., Groundwater recharge in urban areas, Atmos. Environ., 1990, vol. 24, pp. 29‒33.

    Article  Google Scholar 

  32. Leu, A.O., Cai, C., McIlroy, S.J., Southam, G., Orphan, V.J., Yuan, Z., Hu, S., and Tyson, G.W., Anaerobic methane oxidation coupled to manganese reduction by members of the Methanoperedenaceae, ISME J., 2020, vol. 14, pp. 1030‒1041.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Li, F., Liu, X., Zhang, X., Zhao, D., Liu, H., Zhou, C., and Wang, R., Urban ecological infrastructure: an integrated network for ecosystem services and sustainable urban systems, J. Clean. Prod., 2017, vol. 163, pp. S12‒S18.

    Article  Google Scholar 

  34. Magoč, T. and Salzberg, S.L., FLASH: fast length adjustment of short reads to improve genome assemblies, Bioinformatics, 2011, vol. 27, pp. 2957‒2963.

    Article  PubMed  PubMed Central  Google Scholar 

  35. Martín, S., Márquez, M.C., Sánchez-Porro, C., Mellado, E., Arahal, D.R., and Ventosa, A., Marinobacter lipolyticus sp. nov., a novel moderate halophile with lipolytic activity, Int. J. Syst. Evol. Microbiol., 2003, vol. 53, pp. 1383‒1387.

    Article  PubMed  Google Scholar 

  36. McPhearson, T., Pickett, S.T., Grimm, N.B., Niemelä, J., Alberti, M., Elmqvist, T., Weber, C., Haase, D., Breuste, J., and Qureshi, S., Advancing urban ecology toward a science of cities, Bioscience, 2016, vol. 66, pp. 198‒212.

    Article  Google Scholar 

  37. Mehrshad, M., Rodriguez-Valera, F., Amoozegar, M.A., López-García, P., and Ghai, R., The enigmatic SAR202 cluster up close: shedding light on a globally distributed dark ocean lineage involved in sulfur cycling, ISME J., 2018, vol. 12, pp. 655‒668.

    Article  CAS  PubMed  Google Scholar 

  38. Nelson, W.C. and Stegen, J.C., The reduced genomes of Parcubacteria (OD1) contain signatures of a symbiotic lifestyle, Front. Microbiol., 2015, vol. 6, p. 713.

    Article  PubMed  PubMed Central  Google Scholar 

  39. Orata, F.D., Meier-Kolthoff, J.P., Sauvageau, D., and Stein, L.Y., Phylogenomic analysis of the gammaproteobacterial methanotrophs (order Methylococcales) calls for the reclassification of members at the genus and species levels, Front. Microbiol., 2018, vol. 9, p. 3162.

    Article  PubMed  PubMed Central  Google Scholar 

  40. Paul, M., Wolf, L., Fund, K., Held, I., Winter, J., Eiswirth, M., Gallert, C., and Hoetzl, H., Microbiological condition of urban groundwater in the vicinity of leaky sewer systems, Acta Hydrochim. Hydrobiol., 2004, vol. 32, pp. 351‒360.

    Article  CAS  Google Scholar 

  41. Plummer, J.D. and Long, S.C., Identifying sources of surface water pollution: a toolbox approach, J. Am. Water. Works. Assoc., 2009, vol. 101, no. 9, pp. 75‒88.

    Article  CAS  Google Scholar 

  42. Powell, K.L., Taylor, R.G., Cronin, A.A., Barrett, M.H., Pedley, S., Sellwood, J., Trowsdale, S.A., and Lerner, D.N., Microbial contamination of two urban sandstone aquifers in the UK, Water. Res., 2003, vol. 37, pp. 339‒352.

    Article  CAS  PubMed  Google Scholar 

  43. 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 Acids Res., 2013, vol. 41 (Database issue), pp. D590‒D596.

    Article  CAS  PubMed  Google Scholar 

  44. Rezaei Somee, M., Shavandi, M., Dastgheib, S.M.M., and Amoozegar, M.A., Bioremediation of oil-based drill cuttings by a halophilic consortium isolated from oil-contaminated saline soil, 3 Biotech., 2018, vol. 8, p. 229.

  45. Rognes, T., Flouri, T., Nichols, B., Quince, C., and Mahé, F., VSEARCH: a versatile open source tool for metagenomics, PeerJ, 2016, vol. 4, p. e2584.

    Article  PubMed  PubMed Central  Google Scholar 

  46. Scharping, R.J. and Garey, J.R., Relationship between aquifer biofilms and unattached microbial indicators of urban groundwater contamination, Mol. Ecol., 2021, vol. 30, pp. 324‒342.

    Article  CAS  PubMed  Google Scholar 

  47. Sharp, J.M., The impacts of urbanization on groundwater systems and recharge, Aqua Mundi, 2010, pp. 51‒56. https://doi.org/10.4409/Am-004-10-0008

    Book  Google Scholar 

  48. Singer, E., Webb, E.A., Nelson, W.C., Heidelberg, J.F., Ivanova, N., Pati, A., and Edwards, K.J., Genomic potential of Marinobacter aquaeolei, a biogeochemical “opportunitroph,” Appl. Environ. Microbiol., 2011, vol. 77, pp. 2763‒2771.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Sonthiphand, P., Ruangroengkulrith, S., Mhuantong, W., Charoensawan, V., Chotpantarat, S., and Boonkaew-wan, S., Metagenomic insights into microbial diversity in a groundwater basin impacted by a variety of anthropogenic activities, Environ. Sci. Pollut. Res. Int., 2019, vol. 26, pp. 26765‒26781.

    Article  CAS  PubMed  Google Scholar 

  50. Stahl, D.A. and de la Torre, J.R., Physiology and diversity of ammonia-oxidizing archaea, Annu. Rev. Microbiol., 2012, vol. 66, pp. 83‒101.

    Article  CAS  PubMed  Google Scholar 

  51. Szekeres, E., Chiriac, C.M., Baricz, A., Szőke-Nagy, T., Lung, I., Soran, M.L., Rudi, K., Dragos, N., and Coman, C., Investigating antibiotics, antibiotic resistance genes, and microbial contaminants in groundwater in relation to the proximity of urban areas, Environ. Pollut., 2018, vol. 236, pp. 734‒744.

    Article  CAS  PubMed  Google Scholar 

  52. van Kessel, M.A., Speth, D.R., Albertsen, M., Niel-sen, P.H., Op den Camp, H.J., Kartal, B., Jetten, M.S.M., and Lücker, S., Complete nitrification by a single microorganism, Nature, 2015, vol. 528, pp. 555‒559.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Yakimov, M.M., Denaro, R., Genovese, M., Cappello, S., D’Auria, G., Chernikova, T.N., Timmis, K.N., and Giluliano, L., Natural microbial diversity in superficial sediments of Milazzo Harbor (Sicily) and community successions during microcosm enrichment with various hydrocarbons, Environ. Microbiol., 2005, vol. 7, pp. 1426‒1441.

    Article  CAS  PubMed  Google Scholar 

  54. Yakimov, M.M., Timmis, K.N., and Golyshin, P.N., Obligate oil-degrading marine bacteria, Curr. Opin. Biotechnol., 2007, vol. 18, pp. 257‒266.

    Article  CAS  PubMed  Google Scholar 

  55. Yin, J., Chen, J.C., Wu, Q., and Chen, G.Q., Halophiles, coming stars for industrial biotechnology, Biotechnol. Adv., 2015, vol. 33, pp. 1433‒1442.

    Article  CAS  PubMed  Google Scholar 

  56. Zanini, A., Petrella, E., Sanangelantoni, A.M., Angelo, L., Ventosi, B., Viani, L., Rizzo, P., Remelli, S., Bartoli, M., Bolpagni, R., Chelli, A., Feo, A., Francese, R., Iacumin, P., Menta, C., et al., Groundwater characterization from an ecological and human perspective: an interdisciplinary approach in the Functional Urban Area of Parma, Italy, Rend. Lincei. Sci. Fis. Nat., 2019, vol. 30, pp. 93‒108.

    Article  Google Scholar 

  57. Zare, N., Bonakdarpour, B., Amoozegar, M.A., Sha-vandi, M., Fallah, N., Darabi, S., and Taromsary, N.B., Using enriched water and soil-based indigenous halophilic consortia of an oilfield for the biological removal of organic pollutants in hypersaline produced water generated in the same oilfield, Process. Saf. Environ. Prot., 2019, vol. 127, pp. 151‒161.

    Article  CAS  Google Scholar 

  58. Zhou, N., Keffer, J.L., Polson, S.W., and Chan, C.S., Unraveling Fe(II)-oxidizing mechanisms in a facultative Fe(II) oxidizer, Sideroxydans lithotrophicus strain ES-1, via culturing, transcriptomics, and reverse transcription-quantitative PCR, Appl. Environ. Microbiol., 2022, vol. 88, p. e01595-21.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. Zhu, W.Y., Yang, L., Zhang, Z.T.L., Mu, C.G., Wang, Y., Kou, Y.R., Jiang, G.Q., Yin, M., and Tang S.K., Oceanobacillus salinisoli sp. nov., a bacterium isolated from saline soil of Turpan city in Xinjiang province, north–west China, Arch. Microbiol., 2021, vol. 203, pp. 2919‒2924.

    Article  CAS  PubMed  Google Scholar 

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Funding

The study was supported by the Russian Foundation for Basic Research and the Government of Moscow, project no. 21-34-70027, and the Ministry of Science and Higher Education of the Russian Federation.

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Collection of water samples and their physicochemical characterization, as well as isolation of metagenomic DNA, were carried out by E.V. Gruzdev and V.V. Kadnikov. 16S rRNA gene libraries were sequenced by A.V. Mardanov. Analysis of 16S rRNA gene sequencing results was performed by Sh.A. Begmatov and A.V. Beletsky. Data were analyzed and the article was prepared by E.V. Gruzdev, V.V. Kadnikov, and N.V. Ravin. The project was managed by V.V. Kadnikov. All authors participated in the discussion of the results.

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Correspondence to V. V. Kadnikov.

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Gruzdev, E.V., Begmatov, S.A., Beletsky, A.V. et al. Structure and Seasonal Variability of Microbial Communities of Groundwater in the City of Moscow. Microbiology 92, 192–203 (2023). https://doi.org/10.1134/S0026261722603293

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