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Lactobacillus supports Clostridiales to restrict gut colonization by multidrug-resistant Enterobacteriaceae

Author

Listed:
  • Ana Djukovic

    (Fundación para el Fomento de la Investigación Sanitaria y Biomédica de la Comunitat Valenciana - FISABIO
    Sloan-Kettering Institute)

  • María José Garzón

    (Fundación para el Fomento de la Investigación Sanitaria y Biomédica de la Comunitat Valenciana - FISABIO)

  • Cécile Canlet

    (Toulouse University, INRAE UMR 1331, ENVT, INP-Purpan, Paul Sabatier University)

  • Vitor Cabral

    (Instituto Gulbenkian de Ciência)

  • Rym Lalaoui

    (Aix Marseille Univ, IRD, APHM, MEPHI, IHU-Méditerranée Infection)

  • Marc García-Garcerá

    (University of Lausanne)

  • Julia Rechenberger

    (Technical University of Munich)

  • Marie Tremblay-Franco

    (Toulouse University, INRAE UMR 1331, ENVT, INP-Purpan, Paul Sabatier University)

  • Iván Peñaranda

    (Fundación para el Fomento de la Investigación Sanitaria y Biomédica de la Comunitat Valenciana - FISABIO)

  • Leonor Puchades-Carrasco

    (Instituto de Investigación Sanitaria La Fe)

  • Antonio Pineda-Lucena

    (Instituto de Investigación Sanitaria La Fe
    University of Navarra)

  • Eva María González-Barberá

    (Hospital Universitari i Politècnic La Fe)

  • Miguel Salavert

    (Hospital Universitari i Politècnic La Fe)

  • José Luis López-Hontangas

    (Hospital Universitari i Politècnic La Fe)

  • Miguel Á. Sanz

    (Instituto de Investigación Sanitaria La Fe)

  • Jaime Sanz

    (Hospital Universitari i Politècnic La Fe
    CIBERONC, Instituto Carlos III)

  • Bernhard Kuster

    (Technical University of Munich)

  • Jean-Marc Rolain

    (Aix Marseille Univ, IRD, APHM, MEPHI, IHU-Méditerranée Infection)

  • Laurent Debrauwer

    (Toulouse University, INRAE UMR 1331, ENVT, INP-Purpan, Paul Sabatier University)

  • Karina B. Xavier

    (Instituto Gulbenkian de Ciência)

  • Joao B. Xavier

    (Sloan-Kettering Institute)

  • Carles Ubeda

    (Fundación para el Fomento de la Investigación Sanitaria y Biomédica de la Comunitat Valenciana - FISABIO
    Centers of Biomedical Research Network (CIBER) in Epidemiology and Public Health)

Abstract

Infections by multidrug-resistant Enterobacteriaceae (MRE) are life-threatening to patients. The intestinal microbiome protects against MRE colonization, but antibiotics cause collateral damage to commensals and open the way to colonization and subsequent infection. Despite the significance of this problem, the specific commensals and mechanisms that restrict MRE colonization remain largely unknown. Here, by performing a multi-omic prospective study of hospitalized patients combined with mice experiments, we find that Lactobacillus is key, though not sufficient, to restrict MRE gut colonization. Lactobacillus rhamnosus and murinus increase the levels of Clostridiales bacteria, which induces a hostile environment for MRE growth through increased butyrate levels and reduced nutrient sources. This mechanism of colonization resistance, an interaction between Lactobacillus spp. and Clostridiales involving cooperation between microbiota members, is conserved in mice and patients. These results stress the importance of exploiting microbiome interactions for developing effective probiotics that prevent infections in hospitalized patients.

Suggested Citation

  • 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.
  • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-33313-w
    DOI: 10.1038/s41467-022-33313-w
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    References listed on IDEAS

    as
    1. Martina Sassone-Corsi & Sean-Paul Nuccio & Henry Liu & Dulcemaria Hernandez & Christine T. Vu & Amy A. Takahashi & Robert A. Edwards & Manuela Raffatellu, 2016. "Microcins mediate competition among Enterobacteriaceae in the inflamed gut," Nature, Nature, vol. 540(7632), pages 280-283, December.
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    Cited by:

    1. 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.
    2. 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.
    3. 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.

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