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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
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    References listed on IDEAS

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    1. 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.
    2. 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.
    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.
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