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Metabolic cross-feeding in imbalanced diets allows gut microbes to improve reproduction and alter host behaviour

Author

Listed:
  • Sílvia F. Henriques

    (Champalimaud Centre for the Unknown)

  • Darshan B. Dhakan

    (Champalimaud Centre for the Unknown)

  • Lúcia Serra

    (Champalimaud Centre for the Unknown)

  • Ana Patrícia Francisco

    (Champalimaud Centre for the Unknown)

  • Zita Carvalho-Santos

    (Champalimaud Centre for the Unknown)

  • Célia Baltazar

    (Champalimaud Centre for the Unknown)

  • Ana Paula Elias

    (Champalimaud Centre for the Unknown)

  • Margarida Anjos

    (Champalimaud Centre for the Unknown)

  • Tong Zhang

    (University of Glasgow Institute of Cancer Sciences, Switchback Road)

  • Oliver D. K. Maddocks

    (University of Glasgow Institute of Cancer Sciences, Switchback Road)

  • Carlos Ribeiro

    (Champalimaud Centre for the Unknown)

Abstract

The impact of commensal bacteria on the host arises from complex microbial-diet-host interactions. Mapping metabolic interactions in gut microbial communities is therefore key to understand how the microbiome influences the host. Here we use an interdisciplinary approach including isotope-resolved metabolomics to show that in Drosophila melanogaster, Acetobacter pomorum (Ap) and Lactobacillus plantarum (Lp) a syntrophic relationship is established to overcome detrimental host diets and identify Ap as the bacterium altering the host’s feeding decisions. Specifically, we show that Ap uses the lactate produced by Lp to supply amino acids that are essential to Lp, allowing it to grow in imbalanced diets. Lactate is also necessary and sufficient for Ap to alter the fly’s protein appetite. Our data show that gut bacterial communities use metabolic interactions to become resilient to detrimental host diets. These interactions also ensure the constant flow of metabolites used by the microbiome to alter reproduction and host behaviour.

Suggested Citation

  • Sílvia F. Henriques & Darshan B. Dhakan & Lúcia Serra & Ana Patrícia Francisco & Zita Carvalho-Santos & Célia Baltazar & Ana Paula Elias & Margarida Anjos & Tong Zhang & Oliver D. K. Maddocks & Carlos, 2020. "Metabolic cross-feeding in imbalanced diets allows gut microbes to improve reproduction and alter host behaviour," Nature Communications, Nature, vol. 11(1), pages 1-15, December.
    • Handle: RePEc:nat:natcom:v:11:y:2020:i:1:d:10.1038_s41467-020-18049-9
    DOI: 10.1038/s41467-020-18049-9
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    Cited by:

    1. 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.
    2. 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.
    3. Ruohong Wang & Yandong Yin & Jingshu Li & Hongmiao Wang & Wanting Lv & Yang Gao & Tangci Wang & Yedan Zhong & Zhiwei Zhou & Yuping Cai & Xiaoyang Su & Nan Liu & Zheng-Jiang Zhu, 2022. "Global stable-isotope tracing metabolomics reveals system-wide metabolic alternations in aging Drosophila," Nature Communications, Nature, vol. 13(1), pages 1-14, December.

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