Skip to main content

Advertisement

SpringerLink
Log in

Short-term copper exposure as a selection pressure for antibiotic resistance and metal resistance in an agricultural soil

  • Research Article
  • Published:
Environmental Science and Pollution Research Aims and scope Submit manuscript

Abstract

Owing to the similar mechanisms of antibiotic and metal resistance, there is a growing concern that metal contamination may select for antibiotic resistance genes (ARGs) in the environment. Here, we constructed short-term laboratory microcosms to investigate the dynamics of a wide range of ARGs and two copper (Cu) resistance genes in an agricultural soil amended with a gradient of Cu concentrations (0~1000 mg kg−1). Mobile genetic elements (MGEs) were also quantified as a proxy for the horizontal gene transfer potential of ARGs. We detected 126 unique ARGs across all the soil samples using the high-capacity quantitative PCR array, and multidrug and β-lactam resistance were the most abundant ARG categories. The copper amendments significantly enhanced the absolute and relative abundances of ARGs and MGEs, which gradually increased along the gradient of increasing Cu concentrations. The two Cu resistance genes (copA and pcoR) were highly enriched in low-level Cu treatment (50 and 100 mg kg−1), and their abundances decreased with the increasing Cu concentrations. The level of metal and antibiotic resistance gradually declined over time in all Cu-amended treatments but was still considerably higher in contaminated soils than untreated soils after 56 days’ incubation. Significant associations among ARGs and MGEs were revealed by the network analysis, suggesting the mobility potential of antibiotic resistance in Cu-amended soils. No significant positive correlations were found between ARGs and copper resistance genes, suggesting that these genes are not located in the same bacterial hosts. Taken together, our results provide empirical evidence that short-term copper stress can cause evolution of high-level antibiotic and metal resistance and significantly change the diversity, abundance, and horizontal transfer potential of soil ARGs.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Amachawadi RG, Scott HM, Alvarado CA, Mainini TR, Vinasco J, Drouillard JS, Nagaraja TG (2013) Occurrence of the transferable copper resistance gene tcrB, among fecal enterococci of U.S. feedlot cattle fed copper supplemented diets. Appl Environ Microbiol 79:4369–4375

    Article  CAS  Google Scholar 

  • Aminov RI (2011) Horizontal gene exchange in environmental microbiota. Front Microbiol 2:158

    Article  Google Scholar 

  • Ashbolt NHJ, Amezquita A, Backhaus T, Borriello P, Brandt KK, Collignon P (2013) Human health risk assessment (HHRA) for environmental development and transfer of antibiotic resistance. Environ Health Perspect 121:993–1001

    Article  Google Scholar 

  • Baker-Austin C, Wright MS, Stepanauskas R, McArthur JV (2006) Co-selection of antibiotic and metal resistance. Trends Microbiol 14:176–182

    Article  CAS  Google Scholar 

  • Bastian M, Heymann S, Jacomy M (2009) Gephi: an open source software for exploring and manipulating networks. Icwsm 8:361–362

    Google Scholar 

  • Berendonk TU, Manaia CM, Merlin C, Fatta-Kassinos D, Cytryn E, Walsh F, Bürgmann H, Sørum H, Norström M, Pons MN, Kreuzinger N, Huovinen P, Stefani S, Schwartz T, Kisand V, Baquero F, Martinez JL (2015) Tackling antibiotic resistance: the environmental framework. Nat Rev Microbiol 13:310–317

    Article  CAS  Google Scholar 

  • Berg J, Tom-Petersen A, Nybroe O (2005) Copper amendment of agricultural soil selects for bacterial antibiotic resistance in the field. Lett Appl Microbiol 40:146–151

    Article  CAS  Google Scholar 

  • Besaury L, Pawlak B, Quillet L (2016) Expression of copper-resistance genes in microbial communities under copper stress and oxic/anoxic conditions. Environ Sci Pollut Res Int 23:4013–4023

    Article  CAS  Google Scholar 

  • Burch TR, Sadowsky MJ, Lapara TM (2013) Aerobic digestion reduces the quantity of antibiotic resistance genes in residual municipal wastewater solids. Front Microbiol 4:17

    Article  Google Scholar 

  • Chen Q, An X, Li H, Su J, Ma Y, Zhu YG (2016) Long-term field application of sewage sludge increases the abundance of antibiotic resistance genes in soil. Environ Int 92:1–10

    Article  Google Scholar 

  • Chen Q, An X, Zhu YG, Su JQ, Gillings MR, Ye ZL, Cui L (2017) Application of struvite alters the antibiotic resistome in soil, rhizosphere, and phyllosphere. Environ Sci Technol 51:8149–8157

    Article  CAS  Google Scholar 

  • Forsberg KJ, Reyes A, Wang B, Selleck EM, Sommer MOA, Dantas G (2012) The shared antibiotic resistome of soil bacteria and human pathogen. Science 337:1107–1111

    Article  CAS  Google Scholar 

  • Gillings MR, Gaze WH, Pruden A, Smalla K, Tiedje JM, Zhu YG (2015) Using the class 1 integron-integrase gene as a proxy for anthropogenic pollution. ISME J 9:1269–1279

    Article  CAS  Google Scholar 

  • Gou M, Hu HW, Zhang YJ, Wang JT, Hayden H, Tang YQ, He JZ (2018) Aerobic composting reduces antibiotic resistance genes in cattle manure and the resistome dissemination in agricultural soils. Sci Total Environ 612:1300–1310

    Article  CAS  Google Scholar 

  • Han X-M, Hu H-W, Shi X-Z, Wang J-T, Han L-L, Chen D, He J-Z (2016) Impacts of reclaimed water irrigation on soil antibiotic resistome in urban parks of Victoria, Australia. Environmental Pollution 211:48-57

    Article  CAS  Google Scholar 

  • Hu HW, Han XM, Shi XZ, Wang JT, Han LL, Chen D, He JZ (2016a) Temporal changes of antibiotic resistance genes and bacterial communities in two contrasting soils treated with cattle manure. FEMS Microbiol Ecol 92:fiv196

    Article  Google Scholar 

  • Hu HW, Wang JT, Li J, Li JJ, Ma YB, Chen D, He JZ (2016b) Field-based evidence for copper contamination induced changes of antibiotic resistance in agricultural soils. Environ Microbiol 18:3896–3909

    Article  CAS  Google Scholar 

  • Hu HW, Wang JT, Li J, Shi XZ, Ma Y, Chen D, He JZ (2017) Long-term nickel contamination increases the occurrence of antibiotic resistance genes in agricultural soils. Environ Sci Technol 51:790–800

    Article  CAS  Google Scholar 

  • Hu HW, Wang JT, Singh BK, Liu YR, Chen YL, Zhang YJ, He JZ (2018) Diversity of herbaceous plants and bacterial communities regulates soil resistome across forest biomes. Environ Microbiol. https://doi.org/10.1111/1462-2920.14248

  • Ji X, Shen Q, Liu F, Ma J, Xu G, Wang Y, Wu M (2012) Antibiotic resistance gene abundances associated with antibiotics and heavy metals in animal manures and agricultural soils adjacent to feedlots in Shanghai; China. J Hazard Mater 235:178–185

    Article  Google Scholar 

  • Johnson TA, Stedtfeld RD, Wang Q, Cole JR, Hashsham SA, Looft T, Zhu YG, James MT (2016) Clusters of antibiotic resistance genes enriched together stay together in swine agriculture. mBio 7:e02214–e02215

    CAS  Google Scholar 

  • Knapp CW, McCluskey SM, Singh BK, Campbell CD, Hudson G, Graham DW (2011) Antibiotic resistance gene abundances correlate with metal and geochemical conditions in archived Scottish soils. PLoS One 6:1–6

    Article  Google Scholar 

  • Li XF, Yin HB, Su JQ (2012) An attempt to quantify Cu-resistant microorganisms in a paddy soil from Jiaxing, China. Pedosphere 22:201–205

    Article  CAS  Google Scholar 

  • Li LG, Xia Y, Zhang T (2017) Co-occurrence of antibiotic and metal resistance genes revealed in complete genome collection. ISME J 11:651–662

    Article  CAS  Google Scholar 

  • Looft T, Johnson TA, Allen HK, Bayles DO, Alt DP, Stedtfeld RD, Sul WJ, Stedtfeld TM, Chai B, Cole JR (2012) In-feed antibiotic effects on the swine intestinal microbiome. Proc Natl Acad Sci U S A 109:1691–1696

    Article  CAS  Google Scholar 

  • Martinez JL (2009) Environmental pollution by antibiotics and by antibiotic resistance determinants. Environ Pollut 157:2893–2902

    Article  CAS  Google Scholar 

  • Medardus JJ, Molla BZ, Nicol M, Morrow WM, Rajala-Schultz PJ, Kazwala R, Gebreyes WA (2014) In-feed use of heavy metal micronutrients in US swine production systems and its role in persistence of multidrug-resistant salmonellae. Appl Environ Microbiol 80:2317–2325

    Article  Google Scholar 

  • Nesme J, Cecillon S, Delmont TO, Monier JM, Vogel TM, Simont P (2014) Large-scale metagenomic-based study of antibiotic resistance in the environment. Curr Biol 24:1096–1100

    Article  CAS  Google Scholar 

  • Pal C, Bengtsson-Palme J, Kristiansson E, Larsson DJ (2015) Co-occurrence of resistance genes to antibiotics, biocides and metals reveals novel insights into their co-selection potential. BMC Genomics 16:964

    Article  Google Scholar 

  • Poole K (2017) At the nexus of antibiotics and metals: the impact of Cu and Zn on antibiotic activity and resistance. Trends Microbiol 25:820–832

    Article  CAS  Google Scholar 

  • Pruden A, Pei R, Storteboom H, Carlson KH (2006) Antibiotic resistance genes as emerging contaminants: studies in Northern Colorado. Environ Sci Technol 40:7445–7450

    Article  CAS  Google Scholar 

  • Rizzo L, Manaia C, Merlin C, Schwartz T, Dagot C, Ploy MC, Michael I, Fatta-Kassinos D (2013) Urban wastewater treatment plants as hotspots for antibiotic resistant bacteria and genes spread into the environment: a review. Sci Total Environ 447:345–360

    Article  CAS  Google Scholar 

  • Schmittgen TD, Livak JK (2008) Analyzing real-time PCR data by the comparative CT method. Nat Protoc 3:1101–1108

    Article  CAS  Google Scholar 

  • Seiler C, Berendonk TU (2012) Heavy metal driven co-selection of antibiotic resistance in soil and water bodies impacted by agriculture and aquaculture. Front Miciobiol 3:399

    Google Scholar 

  • Sentchilo V, Mayer AP, Guy L, Miyazaki R, Tringe SG, Barry K et al (2013) Community-wide plasmid gene mobilization and selection. ISME J 7:1173–1186

    Article  CAS  Google Scholar 

  • Silveira E, Freitas AR, Antunes P, Barros M, Campos J, Coque TM, Peixe L, Novais C (2014) Co-transfer of resistance to high concentrations of copper and first-line antibiotics among Enterococcus from different origins (humans, animals, the environment and foods) and clonal lineages. J Antimicrob Chemother 69:899–906

    Article  CAS  Google Scholar 

  • Soffer N, Zaneveld J, Thurber RV (2015) Phage-bacteria network analysis and its implication for the understanding of coral disease. Environ Microbiol 17:1203–1218

    CAS  Google Scholar 

  • Stepanauskas R, Glenn TC, Jagoe CH, Tuckfield RC, Lindell AH, King CJ, McArthur JV (2006) Coselection for microbial resistance to metals and antibiotics in freshwater microcosms. Environ Microbiol 8:1510–1514

    Article  CAS  Google Scholar 

  • Su JQ, Wei B, Ou-Yang WY, Huang FY, Zhao Y, Xu HJ, Zhu YG (2015) Antibiotic resistome and its association with bacterial communities during sewage sludge composting. Environ Sci Technol 49:7356–7363

    Article  CAS  Google Scholar 

  • Suzuki MT, Taylor LT, Delong EF (2000) Quantitative analysis of small-subunit rRNA genes in mixed microbial populations via 50-nuclease assays. Appl Environ Microbiol 66:4605–4614

    Article  CAS  Google Scholar 

  • Trajanovska S, Britz ML, Bhave M (1997) Detection of heavy metal ion resistance in Gram-positive and Gram-negative bacteria isolated from lead-contaminated site. Biodegradation 8:113–124

    Article  CAS  Google Scholar 

  • Wang R, Zhang J, Sui Q, Wan H, Tong J, Chen M, Wei Y, Wei D (2016) Effect of red mud addition on tetracycline and copper resistance genes and microbial community during the full scale swine manure composting. Bioresour Technol 216:1049–1057

    Article  CAS  Google Scholar 

  • Yin Y, Gu J, Wang X, Song W, Zhang K, Sun W, Zhang X, Zhang Y, Li H (2017) Effects of copper addition on copper resistance, antibiotic resistance genes, and intl1 during swine manure composting. Front Microbiol 8:344

    Google Scholar 

  • Zhang YJ, Hu HW, Gou M, Wang JT, Chen D, He JZ (2017) Temporal succession of soil antibiotic resistance genes following application of swine, cattle and poultry manures spiked with or without antibiotics. Environ Pollut 231:1621–1632

    Article  CAS  Google Scholar 

  • Zhang ML, Chen LH, Ye CS, Yu X (2018) Co-selection of antibiotic resistance via copper shock loading on bacteria from a drinking water bio-filter. Environ Pollut 233:132–141

    Article  CAS  Google Scholar 

  • Zhu YG, Johnson TA, Su JQ, Qiao M, Guo GX, Stedtfeld RD, Hashsham SA, Tiedje JM (2013) Diverse and abundant antibiotic resistance genes in Chinese swine farms. Proc Natl Acad Sci U S A 110:3435–3440

    Article  CAS  Google Scholar 

  • Zhu YG, Zhao Y, Li B, Huang CL, Zhang SY, Yu S, Chen YS, Zhang T, Gillings MR, Su JQ (2017) Continental-scale pollution of estuaries with antibiotic resistance genes. Nat Microbiol 2:16270

    Article  CAS  Google Scholar 

Download references

Funding

This study was supported by Australian Research Council (DP170103628) and Australian-China Joint Research Centre (ACSRF48165).

Author information

Authors and Affiliations

  1. Faculty of Veterinary and Agricultural Science, The University of Melbourne, Parkville, VIC, 3010, Australia

    Wei Kang, Yu-Jing Zhang, Ji-Zheng He & Hang-Wei Hu

  2. School of Environmental Science and Engineering, Hubei Polytechnic University, Huangshi, 435003, China

    Wei Kang

  3. Key Laboratory for Humid Subtropical Eco-geographical Processes of the Ministry of Education, Fujian Normal University, Fuzhou, 350007, China

    Xiuzhen Shi

Authors
  1. Wei Kang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Yu-Jing Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Xiuzhen Shi
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Ji-Zheng He
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Hang-Wei Hu
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Hang-Wei Hu.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Responsible editor: Diane Purchase

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kang, W., Zhang, YJ., Shi, X. et al. Short-term copper exposure as a selection pressure for antibiotic resistance and metal resistance in an agricultural soil. Environ Sci Pollut Res 25, 29314–29324 (2018). https://doi.org/10.1007/s11356-018-2978-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-018-2978-y

Keywords

Search

Navigation