IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v15y2024i1d10.1038_s41467-023-44272-1.html
   My bibliography  Save this article

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
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-023-44272-1
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-023-44272-1?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    References listed on IDEAS

    as
    1. 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.
    2. 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.
    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.
    Full references (including those not matched with items on IDEAS)

    Citations

    Citations are extracted by the CitEc Project, subscribe to its RSS feed for this item.
    as


    Cited by:

    1. Alexandre Maciel-Guerra & Kubra Babaarslan & Michelle Baker & Aura Rahman & Maqsud Hossain & Abdus Sadique & Jahidul Alam & Salim Uzzaman & Mohammad Ferdous Rahman Sarker & Nasrin Sultana & Ashraful I, 2024. "Core and accessory genomic traits of Vibrio cholerae O1 drive lineage transmission and disease severity," Nature Communications, Nature, vol. 15(1), pages 1-21, December.

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    1. Achal Dhariwal & Polona Rajar & Gabriela Salvadori & Heidi Aarø Åmdal & Dag Berild & Ola Didrik Saugstad & Drude Fugelseth & Gorm Greisen & Ulf Dahle & Kirsti Haaland & Fernanda Cristina Petersen, 2024. "Prolonged hospitalization signature and early antibiotic effects on the nasopharyngeal resistome in preterm infants," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    2. Zakaria Mehrab & Jaiaid Mobin & Ibrahim Asadullah Tahmid & Atif Rahman, 2021. "Efficient association mapping from k-mers—An application in finding sex-specific sequences," PLOS ONE, Public Library of Science, vol. 16(1), pages 1-12, January.
    3. Erki Aun & Age Brauer & Veljo Kisand & Tanel Tenson & Maido Remm, 2018. "A k-mer-based method for the identification of phenotype-associated genomic biomarkers and predicting phenotypes of sequenced bacteria," PLOS Computational Biology, Public Library of Science, vol. 14(10), pages 1-17, October.
    4. Danesh Moradigaravand & Martin Palm & Anne Farewell & Ville Mustonen & Jonas Warringer & Leopold Parts, 2018. "Prediction of antibiotic resistance in Escherichia coli from large-scale pan-genome data," PLOS Computational Biology, Public Library of Science, vol. 14(12), pages 1-17, December.
    5. Jason C. Hyun & Jonathan M. Monk & Richard Szubin & Ying Hefner & Bernhard O. Palsson, 2023. "Global pathogenomic analysis identifies known and candidate genetic antimicrobial resistance determinants in twelve species," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    6. Zhenyan Zhang & Qi Zhang & Tingzhang Wang & Nuohan Xu & Tao Lu & Wenjie Hong & Josep Penuelas & Michael Gillings & Meixia Wang & Wenwen Gao & Haifeng Qian, 2022. "Assessment of global health risk of antibiotic resistance genes," Nature Communications, Nature, vol. 13(1), pages 1-11, December.
    7. Yunyan Zhou & Jingquan Li & Fei Huang & Huashui Ai & Jun Gao & Congying Chen & Lusheng Huang, 2023. "Characterization of the pig lower respiratory tract antibiotic resistome," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    8. Allison L Hicks & Nicole Wheeler & Leonor Sánchez-Busó & Jennifer L Rakeman & Simon R Harris & Yonatan H Grad, 2019. "Evaluation of parameters affecting performance and reliability of machine learning-based antibiotic susceptibility testing from whole genome sequencing data," PLOS Computational Biology, Public Library of Science, vol. 15(9), pages 1-21, September.
    9. Zi-Teng Liu & Rui-Ao Ma & Dong Zhu & Konstantinos T. Konstantinidis & Yong-Guan Zhu & Si-Yu Zhang, 2024. "Organic fertilization co-selects genetically linked antibiotic and metal(loid) resistance genes in global soil microbiome," Nature Communications, Nature, vol. 15(1), pages 1-13, December.

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-023-44272-1. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: Sonal Shukla or Springer Nature Abstracting and Indexing (email available below). General contact details of provider: http://www.nature.com .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.