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Microbiome-mediated fructose depletion restricts murine gut colonization by vancomycin-resistant Enterococcus

Author

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  • Sandrine Isaac

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

  • Alejandra Flor-Duro

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

  • Gloria Carruana

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

  • Leonor Puchades-Carrasco

    (Drug Discovery Unit, Instituto de Investigación Sanitaria La Fe)

  • Anna Quirant

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

  • Marina Lopez-Nogueroles

    (Analytical Unit Platform, Instituto de Investigación Sanitaria La Fe)

  • Antonio Pineda-Lucena

    (Drug Discovery Unit, Instituto de Investigación Sanitaria La Fe
    University of Navarra)

  • Marc Garcia-Garcera

    (University of Lausanne)

  • Carles Ubeda

    (Fundación para el Fomento de la Investigación Sanitaria y Biomédica de la Comunitat Valenciana - FISABIO
    CIBER en Epidemiología y Salud Pública)

Abstract

Multidrug-resistant organisms (MDRO) are a major threat to public health. MDRO infections, including those caused by vancomycin-resistant Enterococcus (VRE), frequently begin by colonization of the intestinal tract, a crucial step that is impaired by the intestinal microbiota. However, the specific members of the microbiota that suppress MDRO colonization and the mechanisms of such protection are largely unknown. Here, using metagenomics and mouse models that mimic the patients’ exposure to antibiotics, we identified commensal bacteria associated with protection against VRE colonization. We further found a consortium of five strains that was sufficient to restrict VRE gut colonization in antibiotic treated mice. Transcriptomics in combination with targeted metabolomics and in vivo assays indicated that the bacterial consortium inhibits VRE growth through nutrient depletion, specifically by reducing the levels of fructose, a carbohydrate that boosts VRE growth in vivo. Finally, in vivo RNA-seq analysis of each strain of the consortium in combination with ex vivo and in vivo assays demonstrated that a single bacterium (Olsenella sp.) could recapitulate the effect of the consortium. Our results indicate that nutrient depletion by specific commensals can reduce VRE intestinal colonization, which represents a novel non-antibiotic based strategy to prevent infections caused by this multidrug-resistant organism.

Suggested Citation

  • 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.
  • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-35380-5
    DOI: 10.1038/s41467-022-35380-5
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    References listed on IDEAS

    as
    1. Sohn G. Kim & Simone Becattini & Thomas U. Moody & Pavel V. Shliaha & Eric R. Littmann & Ruth Seok & Mergim Gjonbalaj & Vincent Eaton & Emily Fontana & Luigi Amoretti & Roberta Wright & Silvia Caballe, 2019. "Microbiota-derived lantibiotic restores resistance against vancomycin-resistant Enterococcus," Nature, Nature, vol. 572(7771), pages 665-669, August.
    2. Sushma Kommineni & Daniel J. Bretl & Vy Lam & Rajrupa Chakraborty & Michael Hayward & Pippa Simpson & Yumei Cao & Pavlos Bousounis & Christopher J. Kristich & Nita H. Salzman, 2015. "Bacteriocin production augments niche competition by enterococci in the mammalian gastrointestinal tract," Nature, Nature, vol. 526(7575), pages 719-722, October.
    3. 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.
    4. Katharina Brandl & George Plitas & Coralia N. Mihu & Carles Ubeda & Ting Jia & Martin Fleisher & Bernd Schnabl & Ronald P. DeMatteo & Eric G. Pamer, 2008. "Vancomycin-resistant enterococci exploit antibiotic-induced innate immune deficits," Nature, Nature, vol. 455(7214), pages 804-807, October.
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    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.

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