Abstract—
Soil is not only a habitat of antibiotic-resistant microorganisms and a natural source of antibiotic resistance genes, but also an environment in which clinical determinants of antibiotic resistance may be accumulated and transferred. Quantitative assessment of antibiotic-resistant bacteria in polluted soils used in agriculture and its comparison to the so-called baseline content of resistant bacteria and their resistance genes in the soil is therefore urgent. However, the data on the study of antibiotic-resistant bacteria in pristine soils (with minimal anthropogenic impact) are practically absent. Comparative study was therefore carried out on the spectra of resistance to natural and synthetic antibiotics among gram-negative bacteria isolated from various soils: pristine (Arctic and Antarctic soils); sites with possible pollution (Albic Retisols (IUSS Working Group WRB, 2015) of a woodland park area in the Moscow region), and moderately polluted soils with high mercury content (near the Khaidarkan mercury mine). It was revealed that strains resistant to one or more of the used natural antibiotics, with the exception of tetracycline, were found in all types of biotopes. About one third of the studied strains, both isolated from soils of polar regions with low anthropogenic impact, and from polluted soils near the Khaidarkan mercury mine, exhibited multiple drug resistance. These results suggest that the presence of multiple antibiotic resistance among bacteria is not solely a response to anthropogenic pollution. Bacterial strains with multidrug antibiotic resistance isolated from the biotopes formed in extremely cold conditions belonged mainly to the genera among the representatives of which intrinsic resistance is widespread, due to the specific structure of their cell walls, preventing antibiotic penetration into the cell, and to the presence of various nonspecific efflux systems of release of toxic substances from the cell.
Similar content being viewed by others
REFERENCES
Altschul, S.F., Gish, W., Miller, W., Myers, E.W., and Lipman, D.J., Basic local alignment search tool, J. Mol. Biol., 1990, vol. 215, pp. 403–410.
Ashbolt, N.J., Amézquita, A., Backhaus, T., Borriello, P., Brandt, K.K., Collignon, P., Coors, A., Finley, R., Gaze, W.H., Heberer, T., Lawrence, J.R., Larsson, D.G.J., McEwen, S.A., Ryan, J.J., Schönfeld, J., et al., Human health risk assessment (HHRA) for environmental development and transfer of antibiotic resistance, Environ. Health Perspect., 2013, vol. 121, pp. 993–1001.
Brown, M.G. and Balkwill, D.L., Antibiotic resistance in bacteria isolated from the deep terrestrial surface, Microb. Ecol., 2009, vol. 57, pp. 484–493.
Bulgakova, V.G., Vinogradova, K.A., Orlova, T.I., Kozhevin, P.A., and Polin, A.N., Action of antibiotics as signalling molecules, Antibiot. Khimioter. (Moscow), vol. 59, nos. 1–2, pp. 36–43.
Cytryn, E., The soil resistome: the anthropogenic, the native, and the unknown, Soil Biol. Biochem., 2013, vol. 63, pp. 18–23.
D’Costa, V.M., King, C.E., Kalan, L., Morar, M., Sung, W.W., Schwarz, C., Froese, D., Zazula, G., Calmels, F., and Debruyne, R., Antibiotic resistance is ancient, Nature, 2011, vol. 477, p. 457.
Delcour, A., Outer membrane permeability and antibiotic resistance, Biochim. Biophys. Acta, 2009, vol. 1794, pp. 808–816.
Durso, L.M., Wedin, D.A., Gilley, J.E., Miller, D.N., and Marx, D.B., Assessment of selected antibiotic resistances in ungrazed native Nebraska prairie soils, J. Environ. Qual., 2016, vol. 45, pp. 454–462.
Hayward, J.L., Jackson, A.J., Yost, C.K., Truelstrup, H.L., and Jamieson, R.C., Fate of antibiotic resistance genes in two Arctic tundra wetlands impacted by municipal wastewater, Sci. Total Environ., 2018, vol. 642, pp. 1415–1428.
Heymann, D.L., Prentice, T., and Reinders, L.T., The World Health Report 2007: A Safer Future: Global Public Health Security in the 21st Century, World Health Organization, 2007.
IUSS Working Group WRB. World Reference Base for Soil Resources 2014, update 2015 International soil classification system for naming soils and creating legends for soil maps, Rome: FAO, World Soil Resources Reports, 2015.
Khesin, R.B. and Karasyova, E.V., Mercury-resistant plasmids in bacteria from a mercury and antimony deposit area, Mol. Gen. Genet., 1984, vol. 197, pp. 280–285.
Lane, D.J., 16S/23S rRNA sequencing, in Nucleic Acid Techniques in Bacterial Systematics, Stackebrandt, E. and Goodfellow, M., Eds., New York: Wiley, 1991, pp. 125–175.
Martínez, J.L., Antibiotics and antibiotic resistance genes in natural environments, Science, 2008, vol. 321, pp. 365–367.
Martinez, J.L., Environmental pollution by antibiotics and by antibiotic resistance determinants, Environ. Pollut., 2009, vol. 157, pp. 2893–2902.
Mindlin, S.Z. and Petrova, M.A., On the origin and distribution of antibiotic resistance: permafrost bacteria studies, Mol. Genet. Microbiol. Virol., (Moscow), 2017, vol. 32, pp. 169–179.
Mindlin, S.Z, Petrova, M.A, Gorlenko, Zh.M., Soina, V.S., Khachikian, N.A., and Karaevskaya, E.A., Multidrug-resistant bacteria in permafrost: isolation, biodiversity, phenotypic and genotypic analysis, in New Permafrost and Glacier Research, Krugger, M.I. and Stern, H.P., Hauppauge, Eds. New York: Nova Science, 2009, pp. 89–105.
Mindlin, S.Z., Soina, V.S., Petrova, M.A., and Gorlenko, Zh.M., Isolation of antibiotic resistance bacterial strains from Eastern Siberia permafrost sediments, Russ. J. Genet., 2008, vol. 44, pp. 27–34.
Petrova, M.A., Gorlenko, Zh.M., and Mindlin, S.Z., Molecular structure and translocation of a multiple antibiotic resistance region of a Psychrobacter psychrophilus permafrost strain, FEMS Microbiol. Lett., 2009, vol. 296, pp. 190–197.
Petrova, M.A., Gorlenko, Zh.M., and Mindlin, S.Z., Tn5045, a novel integron-containing antibiotic and chromate resistance transposon isolated from a permafrost bacterium, Res. Microbiol., 2011, vol. 162, pp. 337–345.
Petrova, M.A., Shcherbatova, N.A., Kurakov, A.V., and Mindlin, S.Z., Genomic characterization and integrative properties of phiSMA6 and phiSMA7, two novel filamentous bacteriophages of Stenotrophomonas maltophilia,Arch. Virol., 2014, vol. 159, pp. 1293–1303.
Rothrock, M.J., Keen, P.L., Cook, K.L., Durso, L.M., Franklin, A.M., and Dungan, R.S., How should we be determining background and baseline antibiotic resistance levels in agroecosystem research?, J. Environ. Qual., 2016, vol. 45, pp. 420–431.
Sambrook, J. and Russel, D.W., Molecular Cloning: A Laboratiry Manual, 3rd ed., Cold Spring Harbor, NY: Cold Spring Harbor Laboratory, 2001.
Van Goethem, M.W., Pierneef, R., Bezuidt, O.K., Van De Peer, Y., Cowan, D.A., and Makhalanyane, T.P., A reservoir of “historical”antibiotic resistance genes in remote pristine Antarctic soils, Microbiome, 2018, vol. 6, p. 40.
Williams-Nguyen, J., Sallach, J.B., Bartelt-Hunt, S., Boxall, A.B., Durso, L.M., McLain, J.E., Singer, R.S., Snow, D.D., and Ziles, J.L., Antibiotics and antibiotic resistance in agroecosystems: state of the science, J. Environ. Qual., 2016, vol. 45, pp. 394–406.
Zhao, Y., Cocerva, T., Cox, S., Tardif, S., Su, J.Q., Zhu, Y.G., and Brandt, K.K., Evidence for co-selection of antibiotic resistance genes and mobile genetic elements in metal polluted urban soils, Sci. Total Environ., 2019, vol. 656, pp. 512–520.
Funding
This work was supported by the Russian Foundation for Basic Research, project no. 18-34-00658.
Author information
Authors and Affiliations
Corresponding author
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. Dedyukhina
Rights and permissions
About this article
Cite this article
Kudinova, A.G., Soina, V.S., Maksakova, S.A. et al. Basic Antibiotic Resistance of Bacteria Isolated from Different Biotopes. Microbiology 88, 739–746 (2019). https://doi.org/10.1134/S0026261719050084
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1134/S0026261719050084