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Obligate cross-feeding expands the metabolic niche of bacteria

Nature Ecology & Evolution volume 5, pages 1224–1232 (2021)Cite this article

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Abstract

Bacteria frequently engage in obligate metabolic mutualisms with other microorganisms. However, it remains generally unclear how the resulting metabolic dependencies affect the ecological niche space accessible to the whole consortium relative to the niche space available to its constituent individuals. Here we address this issue by systematically cultivating metabolically dependent strains of different bacterial species either individually or as pairwise cocultures in a wide range of carbon sources. Our results show that obligate cross-feeding is significantly more likely to expand the metabolic niche space of interacting bacterial populations than to contract it. Moreover, niche expansion occurred predominantly between two specialist taxa and correlated positively with the phylogenetic distance between interaction partners. Together, our results demonstrate that obligate cross-feeding can significantly expand the ecological niche space of interacting bacterial genotypes, thus explaining the widespread occurrence of this type of ecological interaction in natural microbiomes.

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Fig. 1: Deformation of niche space in obligate mutualistic interactions.
Fig. 2: Niche expansion is more common than niche contraction.
Fig. 3: Metabolic specialization drives niche deformation.
Fig. 4: Phylogenetic distance between cross-feeding partners predicts niche deformation in cocultures.

Data availability

Raw data are available at https://doi.org/10.5281/zenodo.4818616.

Code availability

The source code for the data analysis is available at https://github.com/LeonardoOna/Obligate-cross-feeding-expands-the-metabolic-niche-of-bacteria.

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Acknowledgements

We thank the entire Kost lab (present and past) for useful discussion and M. Hermann and A. Möhlmeyer for technical assistance. Advice on the construction of auxotrophic strains from J. Gallie (MPI EvoBio) for P. fluorescens and Á. T. Kovács (DTU) for B. subtilis is gratefully acknowledged. This work was funded by the German Research Foundation (priority program SPP1617, KO 3909/2-1: C.K., S.G.; SFB 944, P19: C.K.; KO 3909/4-1: C.K.; TH 831/3-2: K.M.T.) and the Osnabrück University (L.O., S.G., C.K.).

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Author notes

  1. These authors contributed equally: Leonardo Oña, Samir Giri, Neele Avermann.

Authors and Affiliations

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

    Leonardo Oña, Samir Giri, Neele Avermann & Christian Kost

  2. Experimental Ecology and Evolution Research Group, Department of Bioorganic Chemistry, Max Planck Institute for Chemical Ecology, Jena, Germany

    Samir Giri & Christian Kost

  3. Department of Microbiology and Molecular Biology, Justus-Liebig-Universität, Gießen, Germany

    Maximilian Kreienbaum & Kai M. Thormann

Authors
  1. Leonardo Oña
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Contributions

L.O., S.G. and C.K. conceptualized the study. S.G., C.K. and N.A. designed the experiments. S.G., M.K. and K.M.T. constructed strains. N.A. and S.G. performed experiments. L.O. analysed the data. L.O., S.G. and N.A. interpreted the data. L.O., S.G., N.A. and C.K. wrote the manuscript. C.K. provided resources and acquired funding.

Corresponding author

Correspondence to Christian Kost.

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The authors declare no competing interests.

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Peer review information Nature Ecology & Evolution thanks Clare Abreu and the other, anonymous, reviewer(s) for their contribution to the peer review of this work. Peer reviewer reports are available.

Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Extended data

Extended Data Fig. 1 Proportion of all cases of niche expansion, in which cocultures could use a certain carbon source, while none of the two monocultures could grow under the same conditions (that is double niche expansion).

Data for the different threshold levels to define growth and different time points of the experiment are shown.

Extended Data Fig. 2 Expected and observed niche expansion, double niche expansion, and niche contraction per species.

Expected cases were calculated by randomly assigning events (104 times) across species and carbon sources. Bar plots show the number of cases, in which each species is (a) at least one of the two auxotrophic partners that experience niche expansion (green), (b) involved in cases in which both auxotrophic partners experience niche expansion (green), or (c) at least one of the two auxotrophic partners that experience niche contraction (red) in coculture. The vertical light gray and black bar in (a) shows the fraction of cases, where the species experience or induce niche expansion. Asterisks indicate the results of a binomial test comparing expected and observed values (* P < 0.05, ** P < 0.01, *** P < 0.001).

Extended Data Fig. 3 Expected and observed niche expansion, double niche expansion, and niche contraction per amino acid auxotrophy.

Expected cases were calculated by randomly assigning events (104 times) across auxotrophs and carbon sources. Bar plots show the number of cases, where (a) at least one of the two auxotrophic partners or (b) both auxotrophic partners are experiencing niche expansion (green), or (c) at least one of the two auxotrophic partners is experiencing niche contraction (red) in coculture. The vertical gray bar shows the observed number of cases. The vertical light gray and black bar in (a) shows the fraction of cases, where the auxotrophs experience or induce niche expansion. Asterisks indicate the results of a binomial test comparing expected and observed values (* P < 0.05, ** P < 0.01, *** P < 0.001).

Extended Data Fig. 4 Niche expansion is negatively associated with niche contraction.

A linear regression was fitted to the data (blue line, grey area: ±95% confidence interval). The result of a Spearman rank correlation is shown (n = 108).

Extended Data Fig. 5 Monoculture niches and their normalized overlap can predict the magnitude of niche expansion and niche contraction.

a Normalized niche dissimilarity (that is Jaccard distance) strongly predicts niche expansion, while b normalized niche similarity (that is, Jaccard index) strongly predicts niche contraction. The results of Spearman rank correlations are shown (n = 108). A linear regression was fitted to the data (green/ red line, grey area: ±95% confidence interval).

Extended Data Fig. 6 Niche intersection is negatively associated with phylogenetic distance.

A linear regression was fitted to the data (blue line, grey area: ±95% confidence interval). The result of a Spearman rank correlation is shown (n = 108).

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Oña, L., Giri, S., Avermann, N. et al. Obligate cross-feeding expands the metabolic niche of bacteria. Nat Ecol Evol 5, 1224–1232 (2021). https://doi.org/10.1038/s41559-021-01505-0

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