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Convergence of resistance and evolutionary responses in Escherichia coli and Salmonella enterica co-inhabiting chicken farms in China

Author

Listed:
  • Michelle Baker

    (University of Nottingham, College Road, Sutton Bonington)

  • Xibin Zhang

    (Shandong New Hope Liuhe Group Co. Ltd. and Qingdao Key Laboratory of Animal Feed Safety)

  • Alexandre Maciel-Guerra

    (University of Nottingham, College Road, Sutton Bonington)

  • Kubra Babaarslan

    (University of Nottingham, College Road, Sutton Bonington)

  • Yinping Dong

    (China National Center for Food Safety Risk Assessment)

  • Wei Wang

    (China National Center for Food Safety Risk Assessment)

  • Yujie Hu

    (China National Center for Food Safety Risk Assessment)

  • David Renney

    (2, Wychwood Court, Cotswold Business Village, Moreton-in-Marsh)

  • Longhai Liu

    (Shandong Kaijia Food Co. Ltd)

  • Hui Li

    (No. 9, Zhenghe Road, Luolong District, Luoyang City, Henan Province)

  • Maqsud Hossain

    (University of Nottingham, College Road, Sutton Bonington)

  • Stephan Heeb

    (University of Nottingham, East Drive)

  • Zhiqin Tong

    (No. 9, Zhenghe Road, Luolong District, Luoyang City, Henan Province)

  • Nicole Pearcy

    (University of Nottingham, College Road, Sutton Bonington
    University of Nottingham, East Drive)

  • Meimei Zhang

    (Liaoning Provincial Center for Disease Control and Prevention, No. 168, Jinfeng Street, Hunnan District)

  • Yingzhi Geng

    (Liaoning Provincial Center for Disease Control and Prevention, No. 168, Jinfeng Street, Hunnan District)

  • Li Zhao

    (College of Chemistry and Pharmaceutical Sciences, Qingdao Agricultural University, No. 700 Changcheng Road, Chengyang District)

  • Zhihui Hao

    (College of Veterinary Medicine, China Agricultural University, Haidian District)

  • Nicola Senin

    (University of Perugia)

  • Junshi Chen

    (China National Center for Food Safety Risk Assessment)

  • Zixin Peng

    (China National Center for Food Safety Risk Assessment)

  • Fengqin Li

    (China National Center for Food Safety Risk Assessment)

  • Tania Dottorini

    (University of Nottingham, College Road, Sutton Bonington
    Nottingham Ningbo China Beacons of Excellence Research and Innovation Institute, University of Nottingham Ningbo China)

Abstract

Sharing of genetic elements among different pathogens and commensals inhabiting same hosts and environments has significant implications for antimicrobial resistance (AMR), especially in settings with high antimicrobial exposure. We analysed 661 Escherichia coli and Salmonella enterica isolates collected within and across hosts and environments, in 10 Chinese chicken farms over 2.5 years using data-mining methods. Most isolates within same hosts possessed the same clinically relevant AMR-carrying mobile genetic elements (plasmids: 70.6%, transposons: 78%), which also showed recent common evolution. Supervised machine learning classifiers revealed known and novel AMR-associated mutations and genes underlying resistance to 28 antimicrobials, primarily associated with resistance in E. coli and susceptibility in S. enterica. Many were essential and affected same metabolic processes in both species, albeit with varying degrees of phylogenetic penetration. Multi-modal strategies are crucial to investigate the interplay of mobilome, resistance and metabolism in cohabiting bacteria, especially in ecological settings where community-driven resistance selection occurs.

Suggested Citation

  • Michelle Baker & Xibin Zhang & Alexandre Maciel-Guerra & Kubra Babaarslan & Yinping Dong & Wei Wang & Yujie Hu & David Renney & Longhai Liu & Hui Li & Maqsud Hossain & Stephan Heeb & Zhiqin Tong & Nic, 2024. "Convergence of resistance and evolutionary responses in Escherichia coli and Salmonella enterica co-inhabiting chicken farms in China," Nature Communications, Nature, vol. 15(1), pages 1-21, December.
    • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-023-44272-1
    DOI: 10.1038/s41467-023-44272-1
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    References listed on IDEAS

    as
    1. Jian Sun & Xiao-Ping Liao & Alaric W. D’Souza & Manish Boolchandani & Sheng-Hui Li & Ke Cheng & José Luis Martínez & Liang Li & You-Jun Feng & Liang-Xing Fang & Ting Huang & Jing Xia & Yang Yu & Yu-Fe, 2020. "Environmental remodeling of human gut microbiota and antibiotic resistome in livestock farms," Nature Communications, Nature, vol. 11(1), pages 1-11, December.
    2. John A. Lees & Minna Vehkala & Niko Välimäki & Simon R. Harris & Claire Chewapreecha & Nicholas J. Croucher & Pekka Marttinen & Mark R. Davies & Andrew C. Steer & Steven Y. C. Tong & Antti Honkela & J, 2016. "Sequence element enrichment analysis to determine the genetic basis of bacterial phenotypes," Nature Communications, Nature, vol. 7(1), pages 1-8, November.
    3. Erol S. Kavvas & Laurence Yang & Jonathan M. Monk & David Heckmann & Bernhard O. Palsson, 2020. "A biochemically-interpretable machine learning classifier for microbial GWAS," Nature Communications, Nature, vol. 11(1), pages 1-11, December.
    4. An-Ni Zhang & Jeffry M. Gaston & Chengzhen L. Dai & Shijie Zhao & Mathilde Poyet & Mathieu Groussin & Xiaole Yin & Li-Guan Li & Mark C. M. Loosdrecht & Edward Topp & Michael R. Gillings & William P. H, 2021. "An omics-based framework for assessing the health risk of antimicrobial resistance genes," Nature Communications, Nature, vol. 12(1), pages 1-11, December.
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