Bacterial community assembly and antibiotic resistance genes in soils exposed to antibiotics at environmentally relevant concentrations.
Journal
Environmental microbiology
ISSN: 1462-2920
Titre abrégé: Environ Microbiol
Pays: England
ID NLM: 100883692
Informations de publication
Date de publication:
08 2023
08 2023
Historique:
received:
27
02
2023
accepted:
10
03
2023
medline:
3
8
2023
pubmed:
15
3
2023
entrez:
14
3
2023
Statut:
ppublish
Résumé
Understanding how bacterial community assembly and antibiotic resistance genes (ARGs) respond to antibiotic exposure is essential to deciphering the ecological risk of anthropogenic antibiotic pollution in soils. In this study, three loam soils with different land management (unmanured golf course, dairy-manured pasture, and swine-manured cornfield) were spiked with a mixture of 11 antibiotics at the initial concentration of 100 and 1000 μg kg
Identifiants
pubmed: 36916521
doi: 10.1111/1462-2920.16371
doi:
Substances chimiques
Soil
0
Anti-Bacterial Agents
0
Manure
0
Types de publication
Journal Article
Research Support, U.S. Gov't, Non-P.H.S.
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
1439-1450Informations de copyright
© 2023 The Authors. Environmental Microbiology published by Applied Microbiology International and John Wiley & Sons Ltd.
Références
Albright, M.B. & Martiny, J.B. (2018) Dispersal alters bacterial diversity and composition in a natural community. The ISME Journal, 12, 296-299.
Andersson, D.I. & Hughes, D. (2014) Microbiological effects of sublethal levels of antibiotics. Nature Reviews Microbiology, 12, 465-478.
Bahram, M., Hildebrand, F., Forslund, S.K., Anderson, J.L., Soudzilovskaia, N.A., Bodegom, P.M. et al. (2018) Structure and function of the global topsoil microbiome. Nature, 1, 233-237.
Bernier, S. & Surette, M. (2013) Concentration-dependent activity of antibiotics in natural environments. Frontiers in Microbiology, 4, 1-14.
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, 335-336.
Cassini, A., Högberg, L.D., Plachouras, D., Quattrocchi, A., Hoxha, A., Simonsen, G.S. et al. (2019) Attributable deaths and disability-adjusted life-years caused by infections with antibiotic-resistant bacteria in the EU and the European Economic Area in 2015: a population-level modelling analysis. The Lancet Infectious Diseases, 19, 56-66.
Chase, J.M. (2007) Drought mediates the importance of stochastic community assembly. Proceedings of the National Academy of Sciences, 104, 17430-17434.
Chase, J.M., Biro, E.G., Ryberg, W.A. & Smith, K.G. (2009) Predators temper the relative importance of stochastic processes in the assembly of prey metacommunities. Ecology Letters, 12, 1210-1218.
Chase, J.M. & Myers, J.A. (2011) Disentangling the importance of ecological niches from stochastic processes across scales. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences, 366, 2351-2363.
Chave, J. (2004) Neutral theory and community ecology. Ecology Letters, 7, 241-253.
Chen, Z., Zhang, W., Yang, L., Stedtfeld, R.D., Peng, A., Gu, C. et al. (2019) Antibiotic resistance genes and bacterial communities in cornfield and pasture soils receiving swine and dairy manures. Environmental Pollution, 248, 947-957.
Coyotzi, S., Doxey, A.C., Clark, I.D., Lapen, D.R., Van Cappellen, P. & Neufeld, J.D. (2017) Agricultural soil denitrifiers possess extensive nitrite reductase gene diversity. Environmental Microbiology, 19, 1189-1208.
Cycoń, M., Mrozik, A. & Piotrowska-Seget, Z. (2019) Antibiotics in the soil environment-degradation and their impact on microbial activity and diversity. Frontiers in Microbiology, 10, 1-45.
Delgado-Baquerizo, M., Oliverio, A.M., Brewer, T.E., Benavent-González, A., Eldridge, D.J., Bardgett, R.D. et al. (2018) A global atlas of the dominant bacteria found in soil. Science, 359, 320-325.
DeVries, S.L. & Zhang, P. (2016) Antibiotics and the terrestrial nitrogen cycle: a review. Current Pollution Reports, 2, 51-67.
Ding, Y., Zhang, W., Gu, C., Xagoraraki, I. & Li, H. (2011) Determination of pharmaceuticals in biosolids using accelerated solvent extraction and liquid chromatography/tandem mass spectrometry. Journal of Chromatography A, 1218, 10-16.
Fahrenfeld, N., Knowlton, K., Krometis, L.A., Hession, W.C., Xia, K., Lipscomb, E. et al. (2014) Effect of manure application on abundance of antibiotic resistance genes and their attenuation rates in soil: field-scale mass balance approach. Environmental Science & Technology, 48, 2643-2650.
Ferrenberg, S., O'Neill, S.P., Knelman, J.E., Todd, B., Duggan, S., Bradley, D. et al. (2013) Changes in assembly processes in soil bacterial communities following a wildfire disturbance. The ISME Journal, 7, 1102-1111.
Forsberg, K.J., Patel, S., Gibson, M.K., Lauber, C.L., Knight, R., Fierer, N. et al. (2014) Bacterial phylogeny structures soil resistomes across habitats. Nature, 509, 612-616.
Forsberg, K.J., Reyes, A., Wang, B., Selleck, E.M., Sommer, M.O. & Dantas, G. (2012) The shared antibiotic resistome of soil bacteria and human pathogens. Science, 337, 1107-1111.
Green, J.L., Bohannan, B.J. & Whitaker, R.J. (2008) Microbial biogeography: from taxonomy to traits. Science, 320, 1039-1043.
Grenni, P., Ancona, V. & Caracciolo, A.B. (2018) Ecological effects of antibiotics on natural ecosystems: a review. Microchemical Journal, 136, 25-39.
Gullberg, E., Cao, S., Berg, O.G., Ilbäck, C., Sandegren, L., Hughes, D. et al. (2011) Selection of resistant bacteria at very low antibiotic concentrations. PLoS Pathogens, 7, e1002158.
Haller, M.Y., Müller, S.R., McArdell, C.S., Alder, A.C. & Suter, M.J.-F. (2002) Quantification of veterinary antibiotics (sulfonamides and trimethoprim) in animal manure by liquid chromatography-mass spectrometry. Journal of Chromatography A, 952, 111-120.
Hanson, C.A., Fuhrman, J.A., Horner-Devine, M.C. & Martiny, J.B.H. (2012) Beyond biogeographic patterns: processes shaping the microbial landscape. Nature Reviews Microbiology, 10, 497-506.
Hu, H.-W., Han, X.-M., Shi, X.-Z., Wang, J.-T., Han, L.-L., Chen, D. et al. (2016) Temporal changes of antibiotic-resistance genes and bacterial communities in two contrasting soils treated with cattle manure. FEMS Microbiology Ecology, 92, 1-13.
Huang, S., Vieira, S., Bunk, B., Riedel, T., Spröer, C. & Overmann, J. (2016) First complete genome sequence of a subdivision 6 Acidobacterium strain. Genome Announcements, 4, e00469.
Huber, K.J. & Overmann, J. (2018) Vicinamibacteraceae fam. nov., the first described family within the subdivision 6 Acidobacteria. International Journal of Systematic and Evolutionary Microbiology, 68, 2331-2334.
Hurst, J.J., Oliver, J.P., Schueler, J., Gooch, C., Lansing, S., Crossette, E. et al. (2019) Trends in antimicrobial resistance genes in manure blend pits and long-term storage across dairy farms with comparisons to antimicrobial usage and residual concentrations. Environmental Science & Technology, 53, 2405-2415.
Jiang, X., Ellabaan, M.M.H., Charusanti, P., Munck, C., Blin, K., Tong, Y. et al. (2017) Dissemination of antibiotic resistance genes from antibiotic producers to pathogens. Nature Communications, 8, 15784.
Kalam, S., Basu, A., Ahmad, I., Sayyed, R.Z., El-Enshasy, H.A., Dailin, D.J. et al. (2020) Recent understanding of soil Acidobacteria and their ecological significance: a critical review. Frontiers in Microbiology, 11, 1-15.
Kant, R., van Passel, M.W., Palva, A., Lucas, S., Lapidus, A., Glavina del Rio, T. et al. (2011) Genome sequence of Chthoniobacter flavus Ellin428, an aerobic heterotrophic soil bacterium. Journal of Bacteriology, 193, 2902-2903.
Kinney, C.A., Furlong, E.T., Werner, S.L. & Cahill, J.D. (2006) Presence and distribution of wastewater-derived pharmaceuticals in soil irrigated with reclaimed water. Environmental Toxicology and Chemistry, 25, 317-326.
Knapp, C.W., Dolfing, J., Ehlert, P.A. & Graham, D.W. (2009) Evidence of increasing antibiotic resistance gene abundances in archived soils since 1940. Environmental Science & Technology, 44, 580-587.
Kozich, J.J., Westcott, S.L., Baxter, N.T., Highlander, S.K. & Schloss, P.D. (2013) Development of a dual-index sequencing strategy and curation pipeline for analyzing amplicon sequence data on the MiSeq Illumina sequencing platform. Applied and Environmental Microbiology, 79, 5112-5120.
Kreyling, J., Jentsch, A. & Beierkuhnlein, C. (2011) Stochastic trajectories of succession initiated by extreme climatic events. Ecology Letters, 14, 758-764.
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, 5111-5120.
Looft, T., Johnson, T.A., Allen, H.K., Bayles, D.O., Alt, D.P., Stedtfeld, R.D. et al. (2012) In-feed antibiotic effects on the swine intestinal microbiome. Proceedings of the National Academy of Sciences, 109, 1691-1696.
Lyu, J., Yang, L., Zhang, L., Ye, B. & Wang, L. (2020) Antibiotics in soil and water in China-a systematic review and source analysis. Environmental Pollution, 266, 115147.
Nemergut, D.R., Schmidt, S.K., Fukami, T., O'Neill, S.P., Bilinski, T.M., Stanish, L.F. et al. (2013) Patterns and processes of microbial community assembly. Microbiology and Molecular Biology Reviews, 77, 342-356.
Nesme, J. & Simonet, P. (2015) The soil resistome: a critical review on antibiotic resistance origins, ecology and dissemination potential in telluric bacteria. Environmental Microbiology, 17, 913-930.
Ning, D., Yuan, M., Wu, L., Zhang, Y., Guo, X., Zhou, X. et al. (2020) A quantitative framework reveals ecological drivers of grassland microbial community assembly in response to warming. Nature Communications, 11, 4717.
O'neill, J. (2014) Antimicrobial resistance: tackling a crisis for the health and wealth of nations. Review on Antimicrobial Resistance, 20, 1-16.
Podolsky, S.H. (2018) The evolving response to antibiotic resistance (1945-2018). Palgrave Communications, 4, 124.
Pruden, A., Pei, R., Storteboom, H. & Carlson, K.H. (2006) Antibiotic resistance genes as emerging contaminants: studies in northern Colorado. Environmental Science & Technology, 40, 7445-7450.
Raaijmakers, J.M., Weller, D.M. & Thomashow, L.S. (1997) Frequency of antibiotic-producing Pseudomonas spp. in natural environments. Applied and Environmental Microbiology, 63, 881-887.
Romero, D., Traxler, M.F., López, D. & Kolter, R. (2011) Antibiotics as signal molecules. Chemical Reviews, 111, 5492-5505.
Roose-Amsaleg, C. & Laverman, A.M. (2016) Do antibiotics have environmental side-effects? Impact of synthetic antibiotics on biogeochemical processes. Environmental Science and Pollution Research, 23, 4000-4012.
Rousk, J., Bååth, E., Brookes, P.C., Lauber, C.L., Lozupone, C., Caporaso, J.G. et al. (2010) Soil bacterial and fungal communities across a pH gradient in an arable soil. The ISME Journal, 4, 1340-1351.
Sangwan, P., Chen, X., Hugenholtz, P. & Janssen, P.H. (2004) Chthoniobacter flavus gen. nov., sp. nov., the first pure-culture representative of subdivision two, Spartobacteria classis nov., of the phylum Verrucomicrobia. Applied and Environmental Microbiology, 70, 5875-5881.
Schmitt, H., Haapakangas, H. & van Beelen, P. (2005) Effects of antibiotics on soil microorganisms: time and nutrients influence pollution-induced community tolerance. Soil Biology and Biochemistry, 37, 1882-1892.
Schmitt, H., Stoob, K., Hamscher, G., Smit, E. & Seinen, W. (2006) Tetracyclines and tetracycline resistance in agricultural soils: microcosm and field studies. Microbial Ecology, 51, 267-276.
Shade, A., Klimowicz, A.K., Spear, R.N., Linske, M., Donato, J.J., Hogan, C.S. et al. (2013) Streptomycin application has no detectable effect on bacterial community structure in apple orchard soil. Applied & Environmental Microbiology, 79, 6617-6625.
Stegen, J.C., Lin, X., Konopka, A.E. & Fredrickson, J.K. (2012) Stochastic and deterministic assembly processes in subsurface microbial communities. The ISME Journal, 6, 1653-1664.
Tasho, R.P. & Cho, J.Y. (2016) Veterinary antibiotics in animal waste, its distribution in soil and uptake by plants: a review. Science of the Total Environment, 563, 366-376.
Unger, I.M., Goyne, K.W., Kennedy, A.C., Kremer, R.J., McLain, J.E.T. & Williams, C.F. (2013) Antibiotic effects on microbial community characteristics in soils under conservation management practices. Soil Science Society of America Journal, 77, 100-112.
Vellend, M., Srivastava, D.S., Anderson, K.M., Brown, C.D., Jankowski, J.E., Kleynhans, E.J. et al. (2014) Assessing the relative importance of neutral stochasticity in ecological communities. Oikos, 123, 1420-1430.
Walters, K.E., Capocchi, J.K., Albright, M.B.N., Hao, Z., Brodie, E.L. & Martiny, J.B.H. (2022) Routes and rates of bacterial dispersal impact surface soil microbiome composition and functioning. The ISME Journal, 16, 2295-2304.
Wang, N., Guo, X., Yan, Z., Wang, W., Chen, B., Ge, F. et al. (2016) A comprehensive analysis on spread and distribution characteristic of antibiotic resistance genes in livestock farms of southeastern China. PLoS One, 11, e0156889.
Zhang, Y.-J., Hu, H.-W., Gou, M., Wang, J.-T., Chen, D. & He, J.-Z. (2017) Temporal succession of soil antibiotic resistance genes following application of swine, cattle and poultry manures spiked with or without antibiotics. Environmental Pollution, 231, 1621-1632.
Zhao, W., Wang, B. & Yu, G. (2018) Antibiotic resistance genes in China: occurrence, risk, and correlation among different parameters. Environmental Science and Pollution Research, 25, 21467-21482.
Zhou, J., Deng, Y., Zhang, P., Xue, K., Liang, Y., Van Nostrand, J.D. et al. (2014) Stochasticity, succession, and environmental perturbations in a fluidic ecosystem. Proceedings of the National Academy of Sciences, 111, E836-E845.
Zhou, J. & Ning, D. (2017) Stochastic community assembly: does it matter in microbial ecology? Microbiology and Molecular Biology Reviews, 81, 1-32.
Zhu, Y.G., Johnson, T.A., Su, J.Q., Qiao, M., Guo, G.X., Stedtfeld, R.D. et al. (2013) Diverse and abundant antibiotic resistance genes in Chinese swine farms. Proceedings of the National Academy of Sciences of the United States of America, 110, 3435-3440.