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Long-Term Nickel Contamination Increases the Occurrence of Antibiotic Resistance Genes in Agricultural Soils
Open accessAbstract
Heavy metal contamination is assumed to be a selection pressure on antibiotic resistance, but to our knowledge, evidence of the heavy metal-induced changes of antibiotic resistance is lacking on a long-term basis. Using quantitative PCR array and Illumina sequencing, we investigated the changes of a wide spectrum of soil antibiotic resistance genes (ARGs) following 4–5 year nickel exposure (0–800 mg kg –1 ) in two long-term experimental sites. A total of 149 unique ARGs were detected, with multidrug and β-lactam resistance as the most prevailing ARG types. The frequencies and abundance of ARGs tended to increase along the gradient of increasing nickel concentrations, with the highest values recorded in the treatments amended with 400 mg nickel kg –1 soil. The abundance of mobile genetic elements (MGEs) was significantly associated with ARGs, suggesting that nickel exposure might enhance the potential for horizontal transfer of ARGs. Network analysis demonstrated significant associations between ARGs and MGEs, with the integrase intI1 gene having the most frequent interactions with other co-occurring ARGs. The changes of ARGs were mainly driven by nickel bioavailability and MGEs as revealed by structural equation models. Taken together, long-term nickel exposure significantly increased the diversity, abundance, and horizontal transfer potential of soil ARGs.
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Cites
Cytoscape: A software Environment for integrated models of biomolecular interaction networks
Shannon, P., Markiel, A., Ozier, O., Baliga, N. S., Wang, J. T., Ramage, D., Amin, N., Schwikowski, B., & Ideker, T. (2003) · Genome Research · doi:10.1101/gr.1239303 · Cited by 51,888
Self-citationQIIME allows analysis of high-throughput community sequencing data
Caporaso, J. G., Kuczynski, J., Stombaugh, J., Bittinger, K., Bushman, F. D., Costello, E. K., Fierer, N., Peña, A. G., Goodrich, J. K., Gordon, J. I., et al. (2010) · Nature Methods · doi:10.1038/nmeth.f.303 · Cited by 34,887
Analyzing real-time PCR data by the comparative CT method
Schmittgen, T. D., & Livak, K. J. (2008) · Nature Protocols · doi:10.1038/nprot.2008.73 · Cited by 26,190
Naïve Bayesian Classifier for Rapid Assignment of rRNA Sequences into the New Bacterial Taxonomy
Wang, Q., Garrity, G. M., Tiedje, J. M., & Cole, J. R. (2007) · Applied and Environmental Microbiology · doi:10.1128/aem.00062-07 · Cited by 19,885
UPARSE: highly accurate OTU sequences from microbial amplicon reads
Edgar, R. C. (2013) · Nature Methods · doi:10.1038/nmeth.2604 · Cited by 16,707
FLASH: fast length adjustment of short reads to improve genome assemblies
Magoč, T., & Salzberg, S. L. (2011) · Bioinformatics · doi:10.1093/bioinformatics/btr507 · Cited by 15,366
ggplot2: Elegant Graphics for Data Analysis
Wickham, H. (2009) · doi:10.1007/978-0-387-98141-3 · Cited by 14,447
Gephi: An Open Source Software for Exploring and Manipulating Networks
Bastian, M., Heymann, S., & Jacomy, M. (2009) · Proceedings of the International AAAI Conference on Web and Social Media · doi:10.1609/icwsm.v3i1.13937 · Cited by 11,675
Kolpin, D. W., Furlong, E. T., Meyer, M. T., Thurman, E. M., Zaugg, S. D., Barber, L. B., & Buxton, H. T. (2002) · Environmental Science & Technology · doi:10.1021/es011055j · Cited by 7,953
VEGAN, a package of R functions for community ecology
Dixon, P. (2003) · Journal of Vegetation Science · doi:10.1111/j.1654-1103.2003.tb02228.x · Cited by 6,824
McDonald, D., Price, M. N., Goodrich, J., Nawrocki, E. P., DeSantis, T. Z., Probst, A., Andersen, G. L., Knight, R., & Hugenholtz, P. (2012) · The ISME Journal · doi:10.1038/ismej.2011.139 · Cited by 5,064
Lateral gene transfer and the nature of bacterial innovation
Ochman, H., Lawrence, J. G., & Groisman, E. A. (2000) · Nature · doi:10.1038/35012500 · Cited by 3,816
PyNAST: a flexible tool for aligning sequences to a template alignment
Caporaso, J. G., Bittinger, K., Bushman, F. D., DeSantis, T. Z., Andersen, G. L., & Knight, R. (2010) · Bioinformatics · doi:10.1093/bioinformatics/btp636 · Cited by 3,396
Antibiotic resistance is ancient
D’Costa, V. M., King, C. E., Kalan, L., Morar, M., Sung, W. W. L., Schwarz, C., Froese, D., Zazula, G., Calmels, F., Debruyne, R., et al. (2011) · Nature · doi:10.1038/nature10388 · Cited by 2,720
Microbial heavy-metal resistance
Nies, D. H. (1999) · Applied Microbiology and Biotechnology · doi:10.1007/s002530051457 · Cited by 2,512
Diverse and abundant antibiotic resistance genes in Chinese swine farms
Zhu, Y.-G., Johnson, T. A., Su, J.-Q., Qiao, M., Guo, G.-X., Stedtfeld, R. D., Hashsham, S. A., & Tiedje, J. M. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1222743110 · Cited by 2,440
The ecodist Package for Dissimilarity-based Analysis of Ecological Data
Goslee, S. C., & Urban, D. L. (2007) · Journal of Statistical Software · doi:10.18637/jss.v022.i07 · Cited by 2,429
Tackling antibiotic resistance: the environmental framework
Berendonk, T. U., Manaia, C. M., Merlin, C., Fatta-Kassinos, D., Cytryn, E., Walsh, F., Bürgmann, H., Sørum, H., Norström, M., Pons, M.-N., et al. (2015) · Nature Reviews Microbiology · doi:10.1038/nrmicro3439 · Cited by 2,338
Co-selection of antibiotic and metal resistance
Baker-Austin, C., Wright, M. S., Stepanauskas, R., & McArthur, J. V. (2006) · Trends in Microbiology · doi:10.1016/j.tim.2006.02.006 · Cited by 1,883
Computing topological parameters of biological networks
Assenov, Y., Ramírez, F., Schelhorn, S.-E., Lengauer, T., & Albrecht, M. (2008) · Bioinformatics · doi:10.1093/bioinformatics/btm554 · Cited by 1,826
The shared antibiotic resistome of soil bacteria and human pathogens
Forsberg, K. J., Reyes, A., Wang, B., Selleck, E. M., Sommer, M. O. A., & Dantas, G. (2012) · Science · doi:10.1126/science.1220761 · Cited by 1,650
Microbial co-occurrence relationships in the human microbiome
Faust, K., Sathirapongsasuti, J. F., Izard, J., Segata, N., Gevers, D., Raes, J., & Huttenhower, C. (2012) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1002606 · Cited by 1,527
Using the class 1 integron-integrase gene as a proxy for anthropogenic pollution
Gillings, M. R., Gaze, W. H., Pruden, A., Smalla, K., Tiedje, J. M., & Zhu, Y.-G. (2015) · The ISME Journal · doi:10.1038/ismej.2014.226 · Cited by 1,331
Examining the global distribution of dominant archaeal populations in soil
Bates, S. T., Berg-Lyons, D., Caporaso, J. G., Walters, W. A., Knight, R., & Fierer, N. (2011) · The ISME Journal · doi:10.1038/ismej.2010.171 · Cited by 1,322
Bacterial phylogeny structures soil resistomes across habitats
Forsberg, K. J., Patel, S., Gibson, M. K., Lauber, C. L., Knight, R., Fierer, N., & Dantas, G. (2014) · Nature · doi:10.1038/nature13377 · Cited by 1,287
Li, B., Yang, Y., Ma, L., Ju, F., Guo, F., Tiedje, J. M., & Zhang, T. (2015) · The ISME Journal · doi:10.1038/ismej.2015.59 · Cited by 1,238
Antibiotic-Resistant Bugs in the 21st Century — A Clinical Super-Challenge
Arias, C. A., & Murray, B. E. (2009) · New England Journal of Medicine · doi:10.1056/nejmp0804651 · Cited by 1,027
Horizontal gene transfer, genome innovation and evolution
Gogarten, J. P., & Townsend, J. P. (2005) · Nature Reviews Microbiology · doi:10.1038/nrmicro1204 · Cited by 1,020
Seiler, C., & Berendonk, T. U. (2012) · Frontiers in Microbiology · doi:10.3389/fmicb.2012.00399 · Cited by 1,018
Antibiotic resistance gene spread due to manure application on agricultural fields
Heuer, H., Schmitt, H., & Smalla, K. (2011) · Current Opinion in Microbiology · doi:10.1016/j.mib.2011.04.009 · Cited by 985
Antibiotic Resistome and Its Association with Bacterial Communities during Sewage Sludge Composting
Su, J.-Q., Wei, B., Ou-Yang, W.-Y., Huang, F.-Y., Zhao, Y., Xu, H.-J., & Zhu, Y.-G. (2015) · Environmental Science & Technology · doi:10.1021/acs.est.5b01012 · Cited by 890
Chee‐Sanford, J. C., Mackie, R. I., Koike, S., Krapac, I. G., Lin, Y., Yannarell, A. C., Maxwell, S., & Aminov, R. I. (2009) · Journal of Environmental Quality · doi:10.2134/jeq2008.0128 · Cited by 830
Element concentrations in soils and other surficial materials of the conterminous United States
Shacklette, H. T., & Boerngen, J. G. (1984) · Professional Paper · doi:10.3133/pp1270 · Cited by 787
An inventory of trace element inputs to agricultural soils in China
Luo, L., Ma, Y., Zhang, S., Wei, D., & Zhu, Y.-G. (2009) · Journal of Environmental Management · doi:10.1016/j.jenvman.2009.01.011 · Cited by 731
Self-citationHorizontal Gene Exchange in Environmental Microbiota
Aminov, R. I. (2011) · Frontiers in Microbiology · doi:10.3389/fmicb.2011.00158 · Cited by 644
Selection of a Multidrug Resistance Plasmid by Sublethal Levels of Antibiotics and Heavy Metals
Gullberg, E., Albrecht, L. M., Karlsson, C., Sandegren, L., & Andersson, D. I. (2014) · mBio · doi:10.1128/mbio.01918-14 · Cited by 559
Cadmium, Lead, Zinc, Copper, and Nickel in Agricultural Soils of the United States of America
Holmgren, G. G. S., Meyer, M. W., Chaney, R. L., & Daniels, R. B. (1993) · Journal of Environmental Quality · doi:10.2134/jeq1993.00472425002200020015x · Cited by 532
Functional metagenomics reveals diverse β-lactamases in a remote Alaskan soil
Allen, H. K., Moe, L. A., Rodbumrer, J., Gaarder, A., & Handelsman, J. (2009) · The ISME Journal · doi:10.1038/ismej.2008.86 · Cited by 500
Marti, R., Scott, A., Tien, Y.-C., Murray, R., Sabourin, L., Zhang, Y., & Topp, E. (2013) · Applied and Environmental Microbiology · doi:10.1128/aem.01682-13 · Cited by 450
From patterns to causal understanding: Structural equation modeling (SEM) in soil ecology
Eisenhauer, N., Bowker, M. A., Grace, J. B., & Powell, J. R. (2015) · Pedobiologia · doi:10.1016/j.pedobi.2015.03.002 · Cited by 417
Knapp, C. W., McCluskey, S. M., Singh, B. K., Campbell, C. D., Hudson, G., & Graham, D. W. (2011) · PLoS ONE · doi:10.1371/journal.pone.0027300 · Cited by 394
Abou-Shanab, R. A. I., van Berkum, P., & Angle, J. S. (2007) · Chemosphere · doi:10.1016/j.chemosphere.2006.12.051 · Cited by 367
Wu, D., Huang, Z., Yang, K., Graham, D., & Xie, B. (2015) · Environmental Science & Technology · doi:10.1021/es506081z · Cited by 322
Graham, D. W., Olivares-Rieumont, S., Knapp, C. W., Lima, L., Werner, D., & Bowen, E. (2011) · Environmental Science & Technology · doi:10.1021/es102473z · Cited by 303
Coselection for microbial resistance to metals and antibiotics in freshwater microcosms
Stepanauskas, R., Glenn, T. C., Jagoe, C. H., Tuckfield, R. C., Lindell, A. H., King, C. J., & McArthur, J. V. (2006) · Environmental Microbiology · doi:10.1111/j.1462-2920.2006.01091.x · Cited by 300
China Takes Aim at Rampant Antibiotic Resistance
Hvistendahl, M. (2012) · Science · doi:10.1126/science.336.6083.795 · Cited by 261
Hu, H., Wang, J., Li, J., Li, J., Ma, Y., Chen, D., & He, J. (2016) · Environmental Microbiology · doi:10.1111/1462-2920.13370 · Cited by 261
Self-citationMolecular basis of active copper resistance mechanisms in Gram-negative bacteria
Bondarczuk, K., & Piotrowska-Seget, Z. (2013) · Cell Biology and Toxicology · doi:10.1007/s10565-013-9262-1 · Cited by 252
Berg, J., Thorsen, M. K., Holm, P. E., Jensen, J., Nybroe, O., & Brandt, K. K. (2010) · Environmental Science & Technology · doi:10.1021/es101798r · Cited by 236
Clusters of Antibiotic Resistance Genes Enriched Together Stay Together in Swine Agriculture
Johnson, T. A., Stedtfeld, R. D., Wang, Q., Cole, J. R., Hashsham, S. A., Looft, T. P., Zhu, Y., & Tiedje, J. M. (2016) · mBio · doi:10.1128/mbio.02214-15 · Cited by 235
Copper amendment of agricultural soil selects for bacterial antibiotic resistance in the field
Berg, J., Tom-Petersen, A., & Nybroe, O. (2005) · Letters in Applied Microbiology · doi:10.1111/j.1472-765x.2004.01650.x · Cited by 233
Elevated Microbial Tolerance to Metals and Antibiotics in Metal-Contaminated Industrial Environments
Stepanauskas, R., Glenn, T. C., Jagoe, C. H., Tuckfield, R. C., Lindell, A. H., & McArthur, J. V. (2005) · Environmental Science & Technology · doi:10.1021/es048468f · Cited by 213
The elemental constituents of soils
Bowen, H. J. M., Ure, A. M., & Berrow, M. L. (1982) · Environmental Chemistry · doi:10.1039/9781847555991-00094 · Cited by 211
Wright, M. S., Baker-Austin, C., Lindell, A. H., Stepanauskas, R., Stokes, H. W., & McArthur, J. V. (2008) · The ISME Journal · doi:10.1038/ismej.2008.8 · Cited by 191
Spatial Patterns in Antibiotic Resistance among Stream Bacteria: Effects of Industrial Pollution
McArthur, J. V., & Tuckfield, R. C. (2000) · Applied and Environmental Microbiology · doi:10.1128/aem.66.9.3722-3726.2000 · Cited by 156
Bacterial tolerances to metals and antibiotics in metal-contaminated and reference streams
Wright, M. S., Peltier, G. L., Stepanauskas, R., & McArthur, J. V. (2006) · FEMS Microbiology Ecology · doi:10.1111/j.1574-6941.2006.00154.x · Cited by 155
Durso, L. M., Miller, D. N., & Wienhold, B. J. (2012) · PLoS ONE · doi:10.1371/journal.pone.0048325 · Cited by 151
Hu, H., Han, X., Shi, X., Wang, J., Han, L., Chen, D., & He, J. (2015) · FEMS Microbiology Ecology · doi:10.1093/femsec/fiv169 · Cited by 141
Self-citationHeavy Metal Induced Antibiotic Resistance in Bacterium LSJC7
Chen, S., Li, X., Sun, G., Zhang, Y., Su, J., & Ye, J. (2015) · International Journal of Molecular Sciences · doi:10.3390/ijms161023390 · Cited by 128
Phage–bacteria network analysis and its implication for the understanding of coral disease
Soffer, N., Zaneveld, J., & Thurber, R. L. V. (2014) · Environmental Microbiology · doi:10.1111/1462-2920.12553 · Cited by 105
Zinc-induced antibiotic resistance in activated sludge bioreactors
Peltier, E. F., Vincent, J., Finn, C., & Graham, D. W. (2010) · Water Research · doi:10.1016/j.watres.2010.04.041 · Cited by 94
Trace Metal Dynamics in Floodplain Soils of the River Elbe: A Review
Schulz‐Zunkel, C., & Krueger, F. W. (2009) · Journal of Environmental Quality · doi:10.2134/jeq2008.0299 · Cited by 90
Aging of nickel added to soils as predicted by soil pH and time
Ma, Y., Lombi, E., McLaughlin, M. J., Oliver, I. W., Nolan, A. L., Oorts, K., & Smolders, E. (2013) · Chemosphere · doi:10.1016/j.chemosphere.2013.03.013 · Cited by 64
Self-citationAbella, J., Fahy, A., Duran, R., & Cagnon, C. (2015) · FEMS Microbiology Ecology · doi:10.1093/femsec/fiv140 · Cited by 30
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Hung, W.-C., Rugh, M., Feraud, M., Avasarala, S., Kurylo, J., Gutierrez, M., Jimenez, K., Truong, N., Holden, P. A., Grant, S. B., et al. (2022) · Journal of Hazardous Materials · doi:10.1016/j.jhazmat.2021.127469 · Cited by 17
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Metadata
- Authors
- Hu, H.-W., Wang, J.-T., Li, J., Shi, X.-Z., Ma, Y.-B., Chen, D., & He, J.-Z.
- Venue
- Environmental Science & Technology
- Publisher
- American Chemical Society (ACS)
- Published
- 2016-12-23
- Volume
- 51
- Issue
- 2
- Pages
- 790-800
- ISSN
- 0013-936X (ISSN-L)
- 1520-5851
- OpenAlex
- W2566114714
- Cited by
- 312
- References
- 64
- FWCI
- 12.43
- Type
- journal article
- Language
- en
- Open access
- green
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