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Metabolic exchanges are ubiquitous in natural microbial communities

Nature Microbiology volume 8, pages 2244–2252 (2023)Cite this article

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Abstract

Microbial communities drive global biogeochemical cycles and shape the health of plants and animals—including humans. Their structure and function are determined by ecological and environmental interactions that govern the assembly, stability and evolution of microbial communities. A widely held view is that antagonistic interactions such as competition predominate in microbial communities and are ecologically more important than synergistic interactions—for example, mutualism or commensalism. Over the past decade, however, a more nuanced picture has emerged, wherein bacteria, archaea and fungi exist within interactive networks in which they exchange essential and non-essential metabolites. These metabolic interactions profoundly impact not only the physiology, ecology and evolution of the strains involved, but are also central to the functioning of many, if not all, microbiomes. Therefore, we advocate for a balanced view of microbiome ecology that encompasses both synergistic and antagonistic interactions as key forces driving the structure and dynamics within microbial communities.

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Fig. 1: Obligate metabolic interactions are frequently synergistic.
Fig. 2: Metabolic auxotrophies are common in natural microbial communities.
Fig. 3: Evolution of obligate metabolic interactions within microbial communities.
Fig. 4: Synergistic interactions are more context-dependent than antagonistic interactions.

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Data availability

All data are derived from published sources (see Supplementary Tables 1 and 5 for an overview). The raw data used to generate Figs. 1, 2 and 4 are provided in the Supplementary tables that are mentioned in the figure legends. The raw data that were used to calculate the values shown in Fig. 4 are provided at https://zenodo.org/badge/latestdoi/652204203.

Code availability

The code that was used to calculate the values shown in Fig. 4 is provided at https://zenodo.org/badge/latestdoi/652204203.

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Acknowledgements

We thank the entire Kost laboratory for helpful discussions, as well as F. Zorrilla, S. Giri and L. Oña for sharing data and helping with preparing graphs. C.K. is funded by the German Research Foundation (DFG: SFB 944, P19, KO 3909/2-1, KO 3909/4-1, KO 3909/6-1, KO 3909/9-1) and the Volkswagen Foundation (Az: 9B831). K.R.P. acknowledges support from the UK Medical Research Council (project no. MC_UU_00025/11) and European Research Council (ERC; grant agreement no. 866028). Work on microbial metabolic interactions in the Ralser laboratory is funded by the ERC under grant agreement no. ERC-SyG-2020 951475, the Wellcome Trust (IA 200829/Z/16/Z), as well as the Oxford–Berlin Centre for Advanced studies. S.L.G. is funded by SciLifeLab and the Swedish Research Council VR (grant no. 2022-03077). J.F. acknowledges support from the Israel Science Foundation (grants nos. 883/22 and 3395/20) and the Volkswagen Foundation (Az: 9B831).

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Authors and Affiliations

  1. Osnabrück University, Department of Ecology, School of Biology/Chemistry, Osnabrück, Germany

    Christian Kost

  2. Medical Research Council Toxicology Unit, University of Cambridge, Cambridge, UK

    Kiran Raosaheb Patil

  3. Department of Plant Pathology and Microbiology, The Hebrew University of Jerusalem, Rehovot, Israel

    Jonathan Friedman

  4. Department of Ecology, Environment and Plant Sciences, Science for Life Laboratory, Stockholm University, Stockholm, Sweden

    Sarahi L. Garcia

  5. Charité – Universitätsmedizin Berlin, Department of Biochemistry, Berlin, Germany

    Markus Ralser

  6. The Wellcome Centre for Human Genetics, Nuffield Department of Medicine, University of Oxford, Oxford, UK

    Markus Ralser

  7. Max Planck Institute for Molecular Genetics, Berlin, Germany

    Markus Ralser

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Contributions

C.K. performed the literature search with inputs from all authors. C.K. and J.F. analysed the data. C.K., K.R.P., J.F., S.L.G. and M.R. contributed to the writing of the manuscript.

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Correspondence to Christian Kost, Kiran Raosaheb Patil, Jonathan Friedman, Sarahi L. Garcia or Markus Ralser.

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Supplementary Tables

Supplementary Table 1 References and numerical data for Fig. 1b,c. Supplementary Table 2 Source data for Fig. 1b. Supplementary Table 3 Source data for Fig. 1c: co-cultures of kefir-derived strains in milk. Supplementary Table 4 Source data for Fig. 1c: co-cultures of kefir-derived strains on milk agar plates. Supplementary Table 5 References and Supplementary Information for Fig. 2. Besides the references, numerical data and sample size, the type of bacteria, type of auxotrophy, method to detect auxotrophic genotypes and criteria used to call a genotype auxotrophic are indicated. Supplementary Table 6 Source data for Fig. 4a,b. Supplementary Table 7 Source data for Fig. 4c,d.

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Kost, C., Patil, K.R., Friedman, J. et al. Metabolic exchanges are ubiquitous in natural microbial communities. Nat Microbiol 8, 2244–2252 (2023). https://doi.org/10.1038/s41564-023-01511-x

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