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Continental-scale pollution of estuaries with antibiotic resistance genes

Nature Microbiology volume 2, Article number: 16270 (2017) Cite this article

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Abstract

Antibiotic resistance genes (ARGs) have moved from the environmental resistome into human commensals and pathogens, driven by human selection with antimicrobial agents. These genes have increased in abundance in humans and domestic animals, to become common components of waste streams. Estuarine habitats lie between terrestrial/freshwater and marine ecosystems, acting as natural filtering points for pollutants. Here, we have profiled ARGs in sediments from 18 estuaries over 4,000 km of coastal China using high-throughput quantitative polymerase chain reaction, and investigated their relationship with bacterial communities, antibiotic residues and socio-economic factors. ARGs in estuarine sediments were diverse and abundant, with over 200 different resistance genes being detected, 18 of which were found in all 90 sediment samples. The strong correlations of identified resistance genes with known mobile elements, network analyses and partial redundancy analysis all led to the conclusion that human activity is responsible for the abundance and dissemination of these ARGs. Such widespread pollution with xenogenetic elements has environmental, agricultural and medical consequences.

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Figure 1: Distribution of antibiotic resistance genes (ARGs) and mobile genetic elements (MGEs) in estuarine sediment samples along the coast of China.
Figure 2: ARG profiles in estuarine sediments.
Figure 3: Correlation of total absolute abundance of ARGs with total absolute abundance of transposases and that of the class 1 integron-integrase gene (intI1).
Figure 4: Network analysis depicting co-occurrence patterns among antibiotic resistance genes, transposases and the class 1 integron-integrase gene (intI1).
Figure 5: Partial redundancy analysis (pRDA) differentiating the effects of environmental factors, bacterial community and anthropogenic factors (including antibiotic concentration and socio-economic parameters) on ARG structures in Chinese estuary samples.

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Acknowledgements

The authors thank H. Li and Y.-W. Hong for help with sample collection. This study was supported financially by the National Key Research and Development Plan (2016YFD0800205), the Natural Science Foundation of China (21210008), the Knowledge Innovation Program of the Chinese Academy of Sciences (IUEQN201504), the International Science & Technology Cooperation Program of China (2011DFB91710) and Youth Innovation Promotion Association CAS.

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  1. Yong-Guan Zhu and Yi Zhao: These authors contributed equally to this work.

Authors and Affiliations

  1. Key Lab of Urban Environment and Health, Institute of Urban Environment, Chinese Academy of Sciences, 361021, Xiamen, China

    Yong-Guan Zhu, Yi Zhao, Chu-Long Huang, Shen Yu, Yong-Shan Chen & Jian-Qiang Su

  2. State Key Lab of Urban and Regional Ecology, Research Center for Eco-Environmental Sciences, Chinese Academy of Sciences, 100085, Beijing, China

    Yong-Guan Zhu & Si-Yu Zhang

  3. Graduate School at Shenzhen, Tsinghua University, 518055, Shenzhen, China

    Bing Li

  4. Department of Civil Engineering, Environmental Biotechnology Laboratory, University of Hong Kong, Hong Kong SAR, China

    Tong Zhang

  5. Department of Biological Sciences, Genes to Geoscience Research Centre, Macquarie University, Sydney, 2109, New South Wales, Australia

    Michael R. Gillings

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Contributions

Y.-G.Z. and J.-Q.S. designed the project. S.Y. and Y.-S.C. performed sediment sampling. Y.Z. performed ARGs quantification and data analysis with J.Q.S. B.L. conducted network analysis. S.-Y.Z. conducted distance-decay analysis. C.-L.H. and Y.Z. collected the socio-economic data. Y.-G.Z. and Y.Z. wrote the manuscript with contributions from M.R.G. Y.-G.Z., J.-Q.S. and T.Z. provided conceptual advice. J.-Q.S. and M.R.G. revised the paper. All authors discussed and interpreted the results and contributed to the manuscript.

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Correspondence to Yong-Guan Zhu or Jian-Qiang Su.

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Supplementary information

Supplementary Information

Supplementary Tables 1–11; Supplementary Figures 1–15; Supplementary Discussion and Tables. (PDF 1680 kb)

Supplementary Data 1

Normalized gene copy numbers (copies per 4,000 bacterial cells). The data are the ratio of gene copy numbers to 16S gene copy numbers subsequently multiplied by 4,000. (XLSX 38 kb)

Supplementary Data 2

Primer sets (296) used in this study. (XLSX 27 kb)

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Zhu, YG., Zhao, Y., Li, B. et al. Continental-scale pollution of estuaries with antibiotic resistance genes. Nat Microbiol 2, 16270 (2017). https://doi.org/10.1038/nmicrobiol.2016.270

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