IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v14y2023i1d10.1038_s41467-023-38022-6.html
   My bibliography  Save this article

Tradeoff between lag time and growth rate drives the plasmid acquisition cost

Author

Listed:
  • Mehrose Ahmad

    (Barnard College)

  • Hannah Prensky

    (Barnard College)

  • Jacqueline Balestrieri

    (Barnard College)

  • Shahd ElNaggar

    (Barnard College)

  • Angela Gomez-Simmonds

    (Columbia University Medical Center)

  • Anne-Catrin Uhlemann

    (Columbia University Medical Center)

  • Beth Traxler

    (University of Washington)

  • Abhyudai Singh

    (University of Delaware)

  • Allison J. Lopatkin

    (Barnard College
    Columbia University
    Columbia University
    University of Rochester)

Abstract

Conjugative plasmids drive genetic diversity and evolution in microbial populations. Despite their prevalence, plasmids can impose long-term fitness costs on their hosts, altering population structure, growth dynamics, and evolutionary outcomes. In addition to long-term fitness costs, acquiring a new plasmid introduces an immediate, short-term perturbation to the cell. However, due to the transient nature of this plasmid acquisition cost, a quantitative understanding of its physiological manifestations, overall magnitudes, and population-level implications, remains unclear. To address this, here we track growth of single colonies immediately following plasmid acquisition. We find that plasmid acquisition costs are primarily driven by changes in lag time, rather than growth rate, for nearly 60 conditions covering diverse plasmids, selection environments, and clinical strains/species. Surprisingly, for a costly plasmid, clones exhibiting longer lag times also achieve faster recovery growth rates, suggesting an evolutionary tradeoff. Modeling and experiments demonstrate that this tradeoff leads to counterintuitive ecological dynamics, whereby intermediate-cost plasmids outcompete both their low and high-cost counterparts. These results suggest that, unlike fitness costs, plasmid acquisition dynamics are not uniformly driven by minimizing growth disadvantages. Moreover, a lag/growth tradeoff has clear implications in predicting the ecological outcomes and intervention strategies of bacteria undergoing conjugation.

Suggested Citation

  • 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.
  • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-38022-6
    DOI: 10.1038/s41467-023-38022-6
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-023-38022-6
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-023-38022-6?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. 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.
    2. 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.
    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. Andras Gyorgy, 2023. "Competition and evolutionary selection among core regulatory motifs in gene expression control," Nature Communications, Nature, vol. 14(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. 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.
    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. 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.
    4. 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.
    5. 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.
    6. 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.
    7. 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.
    8. 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.
    9. 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.
    10. 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.

    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_s41467-023-38022-6. 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.