IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v14y2023i1d10.1038_s41467-023-40872-z.html
   My bibliography  Save this article

Antibiotics promote intestinal growth of carbapenem-resistant Enterobacteriaceae by enriching nutrients and depleting microbial metabolites

Author

Listed:
  • Alexander Y. G. Yip

    (Imperial College London)

  • Olivia G. King

    (Imperial College London)

  • Oleksii Omelchenko

    (Imperial College London)

  • Sanjana Kurkimat

    (Imperial College London)

  • Victoria Horrocks

    (Imperial College London)

  • Phoebe Mostyn

    (Imperial College London)

  • Nathan Danckert

    (Imperial College London)

  • Rohma Ghani

    (Imperial College London
    Imperial College Healthcare NHS Trust)

  • Giovanni Satta

    (University College London)

  • Elita Jauneikaite

    (Imperial College London
    Imperial College London)

  • Frances J. Davies

    (Imperial College Healthcare NHS Trust)

  • Thomas B. Clarke

    (Imperial College London)

  • Benjamin H. Mullish

    (Imperial College London
    St Mary’s Hospital, Imperial College Healthcare NHS Trust)

  • Julian R. Marchesi

    (Imperial College London)

  • Julie A. K. McDonald

    (Imperial College London)

Abstract

The intestine is the primary colonisation site for carbapenem-resistant Enterobacteriaceae (CRE) and serves as a reservoir of CRE that cause invasive infections (e.g. bloodstream infections). Broad-spectrum antibiotics disrupt colonisation resistance mediated by the gut microbiota, promoting the expansion of CRE within the intestine. Here, we show that antibiotic-induced reduction of gut microbial populations leads to an enrichment of nutrients and depletion of inhibitory metabolites, which enhances CRE growth. Antibiotics decrease the abundance of gut commensals (including Bifidobacteriaceae and Bacteroidales) in ex vivo cultures of human faecal microbiota; this is accompanied by depletion of microbial metabolites and enrichment of nutrients. We measure the nutrient utilisation abilities, nutrient preferences, and metabolite inhibition susceptibilities of several CRE strains. We find that CRE can use the nutrients (enriched after antibiotic treatment) as carbon and nitrogen sources for growth. These nutrients also increase in faeces from antibiotic-treated mice and decrease following intestinal colonisation with carbapenem-resistant Escherichia coli. Furthermore, certain microbial metabolites (depleted upon antibiotic treatment) inhibit CRE growth. Our results show that killing gut commensals with antibiotics facilitates CRE colonisation by enriching nutrients and depleting inhibitory microbial metabolites.

Suggested Citation

  • Alexander Y. G. Yip & Olivia G. King & Oleksii Omelchenko & Sanjana Kurkimat & Victoria Horrocks & Phoebe Mostyn & Nathan Danckert & Rohma Ghani & Giovanni Satta & Elita Jauneikaite & Frances J. Davie, 2023. "Antibiotics promote intestinal growth of carbapenem-resistant Enterobacteriaceae by enriching nutrients and depleting microbial metabolites," Nature Communications, Nature, vol. 14(1), pages 1-20, December.
  • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-40872-z
    DOI: 10.1038/s41467-023-40872-z
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-023-40872-z
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-023-40872-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. Katharine M. Ng & Jessica A. Ferreyra & Steven K. Higginbottom & Jonathan B. Lynch & Purna C. Kashyap & Smita Gopinath & Natasha Naidu & Biswa Choudhury & Bart C. Weimer & Denise M. Monack & Justin L., 2013. "Microbiota-liberated host sugars facilitate post-antibiotic expansion of enteric pathogens," Nature, Nature, vol. 502(7469), pages 96-99, October.
    2. Ana Djukovic & María José Garzón & Cécile Canlet & Vitor Cabral & Rym Lalaoui & Marc García-Garcerá & Julia Rechenberger & Marie Tremblay-Franco & Iván Peñaranda & Leonor Puchades-Carrasco & Antonio P, 2022. "Lactobacillus supports Clostridiales to restrict gut colonization by multidrug-resistant Enterobacteriaceae," Nature Communications, Nature, vol. 13(1), pages 1-18, December.
    3. Casey M. Theriot & Mark J. Koenigsknecht & Paul E. Carlson & Gabrielle E. Hatton & Adam M. Nelson & Bo Li & Gary B. Huffnagle & Jun Z. Li & Vincent B. Young, 2014. "Antibiotic-induced shifts in the mouse gut microbiome and metabolome increase susceptibility to Clostridium difficile infection," Nature Communications, Nature, vol. 5(1), pages 1-10, May.
    Full references (including those not matched with items on IDEAS)

    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. Jordy Evan Sulaiman & Jaron Thompson & Yili Qian & Eugenio I. Vivas & Christian Diener & Sean M. Gibbons & Nasia Safdar & Ophelia S. Venturelli, 2024. "Elucidating human gut microbiota interactions that robustly inhibit diverse Clostridioides difficile strains across different nutrient landscapes," Nature Communications, Nature, vol. 15(1), pages 1-20, December.
    2. James D Brunner & Nicholas Chia, 2020. "Minimizing the number of optimizations for efficient community dynamic flux balance analysis," PLOS Computational Biology, Public Library of Science, vol. 16(9), pages 1-20, September.
    3. Giuliano Bonanomi & Mohamed Idbella & Ahmed M. Abd-ElGawad, 2021. "Microbiota Management for Effective Disease Suppression: A Systematic Comparison between Soil and Mammals Gut," Sustainability, MDPI, vol. 13(14), pages 1-16, July.
    4. Rui Xu & Wandy L. Beatty & Valentin Greigert & William H. Witola & L. David Sibley, 2024. "Multiple pathways for glucose phosphate transport and utilization support growth of Cryptosporidium parvum," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    5. Sandrine Isaac & Alejandra Flor-Duro & Gloria Carruana & Leonor Puchades-Carrasco & Anna Quirant & Marina Lopez-Nogueroles & Antonio Pineda-Lucena & Marc Garcia-Garcera & Carles Ubeda, 2022. "Microbiome-mediated fructose depletion restricts murine gut colonization by vancomycin-resistant Enterococcus," Nature Communications, Nature, vol. 13(1), pages 1-19, December.
    6. Ren Dodge & Eric W. Jones & Haolong Zhu & Benjamin Obadia & Daniel J. Martinez & Chenhui Wang & Andrés Aranda-Díaz & Kevin Aumiller & Zhexian Liu & Marco Voltolini & Eoin L. Brodie & Kerwyn Casey Huan, 2023. "A symbiotic physical niche in Drosophila melanogaster regulates stable association of a multi-species gut microbiota," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    7. Vinod Nikhra, 2019. "Therapeutic Potential of Gut Microbiome Manipulation: Concepts in Fecal Microbiota Transplantation," Current Research in Diabetes & Obesity Journal, Juniper Publishers Inc., vol. 11(1), pages 1-9, June.
    8. Emily C Woods & Adrianne N Edwards & Kevin O Childress & Joshua B Jones & Shonna M McBride, 2018. "The C. difficile clnRAB operon initiates adaptations to the host environment in response to LL-37," PLOS Pathogens, Public Library of Science, vol. 14(8), pages 1-28, August.
    9. Naomi Ohta & Bo Norby & Guy H Loneragan & Javier Vinasco & Henk C den Bakker & Sara D Lawhon & Keri N Norman & Harvey M Scott, 2019. "Quantitative dynamics of Salmonella and E. coli in feces of feedlot cattle treated with ceftiofur and chlortetracycline," PLOS ONE, Public Library of Science, vol. 14(12), pages 1-17, December.
    10. Elvin Koh & In Young Hwang & Hui Ling Lee & Ryan De Sotto & Jonathan Wei Jie Lee & Yung Seng Lee & John C. March & Matthew Wook Chang, 2022. "Engineering probiotics to inhibit Clostridioides difficile infection by dynamic regulation of intestinal metabolism," Nature Communications, Nature, vol. 13(1), pages 1-13, December.
    11. Tomás Clive Barker-Tejeda & Elisa Zubeldia-Varela & Andrea Macías-Camero & Lola Alonso & Isabel Adoración Martín-Antoniano & María Fernanda Rey-Stolle & Leticia Mera-Berriatua & Raphaëlle Bazire & Pau, 2024. "Comparative characterization of the infant gut microbiome and their maternal lineage by a multi-omics approach," Nature Communications, Nature, vol. 15(1), pages 1-21, December.
    12. K. E. Huus & T. T. Hoang & A. Creus-Cuadros & M. Cirstea & S. L. Vogt & K. Knuff-Janzen & P. J. Sansonetti & P. Vonaesch & B. B. Finlay, 2021. "Cross-feeding between intestinal pathobionts promotes their overgrowth during undernutrition," Nature Communications, Nature, vol. 12(1), pages 1-14, December.
    13. Vinod Nikhra, 2019. "Therapeutic Potential of Gut Microbiome Manipulation: Concepts in Fecal Microbiota Transplantation," Current Research in Diabetes & Obesity Journal, Juniper Publishers Inc., vol. 11(1), pages 9-17, June.

    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_s41467-023-40872-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.