IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v14y2023i1d10.1038_s41467-023-39354-z.html
   My bibliography  Save this article

Timing of antibiotic administration determines the spread of plasmid-encoded antibiotic resistance during microbial range expansion

Author

Listed:
  • Yinyin Ma

    (Swiss Federal Institute of Aquatic Science and Technology (Eawag)
    Swiss Federal Institute of Technology (ETH))

  • Josep Ramoneda

    (Swiss Federal Institute of Aquatic Science and Technology (Eawag)
    University of Colorado)

  • David R. Johnson

    (Swiss Federal Institute of Aquatic Science and Technology (Eawag)
    University of Bern)

Abstract

Plasmids are the main vector by which antibiotic resistance is transferred between bacterial cells within surface-associated communities. In this study, we ask whether there is an optimal time to administer antibiotics to minimize plasmid spread in new bacterial genotypes during community expansion across surfaces. We address this question using consortia of Pseudomonas stutzeri strains, where one is an antibiotic resistance-encoding plasmid donor and the other a potential recipient. We allowed the strains to co-expand across a surface and administered antibiotics at different times. We find that plasmid transfer and transconjugant proliferation have unimodal relationships with the timing of antibiotic administration, where they reach maxima at intermediate times. These unimodal relationships result from the interplay between the probabilities of plasmid transfer and loss. Our study provides mechanistic insights into the transfer and proliferation of antibiotic resistance-encoding plasmids within microbial communities and identifies the timing of antibiotic administration as an important determinant.

Suggested Citation

  • Yinyin Ma & Josep Ramoneda & David R. Johnson, 2023. "Timing of antibiotic administration determines the spread of plasmid-encoded antibiotic resistance during microbial range expansion," Nature Communications, Nature, vol. 14(1), pages 1-12, December.
  • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-39354-z
    DOI: 10.1038/s41467-023-39354-z
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-023-39354-z
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-023-39354-z?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. Helmut Hirt & Kerryl E. Greenwood-Quaintance & Aaron M. T. Barnes & Melissa J. Karau & Lisa M. Till & Elise Palzer & Weihua Guan & Michael S. VanNieuwenhze & Purna C. Kashyap & Robin Patel & Gary M. D, 2022. "Dynamics of plasmid-mediated niche invasion, immunity to invasion, and pheromone-inducible conjugation in the murine gastrointestinal tract," Nature Communications, Nature, vol. 13(1), pages 1-10, December.
    2. Erik Bakkeren & Jana S. Huisman & Stefan A. Fattinger & Annika Hausmann & Markus Furter & Adrian Egli & Emma Slack & Mikael E. Sellin & Sebastian Bonhoeffer & Roland R. Regoes & Médéric Diard & Wolf-D, 2019. "Salmonella persisters promote the spread of antibiotic resistance plasmids in the gut," Nature, Nature, vol. 573(7773), pages 276-280, September.
    3. Allison J. Lopatkin & Hannah R. Meredith & Jaydeep K. Srimani & Connor Pfeiffer & Rick Durrett & Lingchong You, 2017. "Persistence and reversal of plasmid-mediated antibiotic resistance," Nature Communications, Nature, vol. 8(1), pages 1-10, December.
    4. Tanita Wein & Nils F. Hülter & Itzhak Mizrahi & Tal Dagan, 2019. "Emergence of plasmid stability under non-selective conditions maintains antibiotic resistance," Nature Communications, Nature, vol. 10(1), pages 1-13, 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. Chujin Ruan & Josep Ramoneda & Anton Kan & Timothy J. Rudge & Gang Wang & David R. Johnson, 2024. "Phage predation accelerates the spread of plasmid-encoded antibiotic resistance," Nature Communications, Nature, vol. 15(1), pages 1-12, 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. Mehrose Ahmad & Hannah Prensky & Jacqueline Balestrieri & Shahd ElNaggar & Angela Gomez-Simmonds & Anne-Catrin Uhlemann & Beth Traxler & Abhyudai Singh & Allison J. Lopatkin, 2023. "Tradeoff between lag time and growth rate drives the plasmid acquisition cost," Nature Communications, Nature, vol. 14(1), pages 1-12, December.
    2. Pengdbamba Dieudonné Zongo & Nicolas Cabanel & Guilhem Royer & Florence Depardieu & Alain Hartmann & Thierry Naas & Philippe Glaser & Isabelle Rosinski-Chupin, 2024. "An antiplasmid system drives antibiotic resistance gene integration in carbapenemase-producing Escherichia coli lineages," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    3. Minghui Cheng & Yingjie Xu & Xiao Cui & Xin Wei & Yundi Chang & Jun Xu & Cheng Lei & Lei Xue & Yifan Zheng & Zhang Wang & Lingtong Huang & Min Zheng & Hong Luo & Yuxin Leng & Chao Jiang, 2024. "Deep longitudinal lower respiratory tract microbiome profiling reveals genome-resolved functional and evolutionary dynamics in critical illness," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    4. Helena R. Ma & Helen Z. Xu & Kyeri Kim & Deverick J. Anderson & Lingchong You, 2024. "Private benefit of β-lactamase dictates selection dynamics of combination antibiotic treatment," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    5. Rohan Maddamsetti & Yi Yao & Teng Wang & Junheng Gao & Vincent T. Huang & Grayson S. Hamrick & Hye-In Son & Lingchong You, 2024. "Duplicated antibiotic resistance genes reveal ongoing selection and horizontal gene transfer in bacteria," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    6. Jia, Jing & Zhao, Zhong & Yang, Jingen & Zeb, Anwar, 2024. "Parameter estimation and global sensitivity analysis of a bacterial-plasmid model with impulsive drug treatment," Chaos, Solitons & Fractals, Elsevier, vol. 183(C).
    7. John P. Marken & Richard M. Murray, 2023. "Addressable and adaptable intercellular communication via DNA messaging," Nature Communications, Nature, vol. 14(1), pages 1-11, December.
    8. Alvah Zorea & David Pellow & Liron Levin & Shai Pilosof & Jonathan Friedman & Ron Shamir & Itzhak Mizrahi, 2024. "Plasmids in the human gut reveal neutral dispersal and recombination that is overpowered by inflammatory diseases," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    9. Wanli He & Jakob Russel & Franziska Klincke & Joseph Nesme & Søren Johannes Sørensen, 2024. "Insights into the ecology of the infant gut plasmidome," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    10. Xuanji Li & Asker Brejnrod & Jonathan Thorsen & Trine Zachariasen & Urvish Trivedi & Jakob Russel & Gisle Alberg Vestergaard & Jakob Stokholm & Morten Arendt Rasmussen & Søren Johannes Sørensen, 2023. "Differential responses of the gut microbiome and resistome to antibiotic exposures in infants and adults," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    11. Shiben Zhu & Juken Hong & Teng Wang, 2024. "Horizontal gene transfer is predicted to overcome the diversity limit of competing microbial species," Nature Communications, Nature, vol. 15(1), pages 1-9, December.
    12. Miles V. Rouches & Yasu Xu & Louis Brian Georges Cortes & Guillaume Lambert, 2022. "A plasmid system with tunable copy number," Nature Communications, Nature, vol. 13(1), pages 1-12, December.
    13. Peter J. Diebold & Matthew W. Rhee & Qiaojuan Shi & Nguyen Vinh Trung & Fayaz Umrani & Sheraz Ahmed & Vandana Kulkarni & Prasad Deshpande & Mallika Alexander & Ngo Hoa & Nicholas A. Christakis & Najee, 2023. "Clinically relevant antibiotic resistance genes are linked to a limited set of taxa within gut microbiome worldwide," Nature Communications, Nature, vol. 14(1), pages 1-12, December.
    14. Xuan Zou & Xiaohong Xiao & Ziran Mo & Yashi Ge & Xing Jiang & Ruolin Huang & Mengxue Li & Zixin Deng & Shi Chen & Lianrong Wang & Sang Yup Lee, 2022. "Systematic strategies for developing phage resistant Escherichia coli strains," Nature Communications, Nature, vol. 13(1), pages 1-12, December.
    15. Erica J. Zheng & Ian W. Andrews & Alexandra T. Grote & Abigail L. Manson & Miguel A. Alcantar & Ashlee M. Earl & James J. Collins, 2022. "Modulating the evolutionary trajectory of tolerance using antibiotics with different metabolic dependencies," Nature Communications, Nature, vol. 13(1), pages 1-11, December.
    16. Qiu E. Yang & Xiaodan Ma & Minchun Li & Mengshi Zhao & Lingshuang Zeng & Minzhen He & Hui Deng & Hanpeng Liao & Christopher Rensing & Ville-Petri Friman & Shungui Zhou & Timothy R. Walsh, 2024. "Evolution of triclosan resistance modulates bacterial permissiveness to multidrug resistance plasmids and phages," 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:14:y:2023:i:1:d:10.1038_s41467-023-39354-z. 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.