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Community composition and the environment modulate the population dynamics of type VI secretion in human gut bacteria

Nature Ecology & Evolution volume 7, pages 2092–2107 (2023)Cite this article

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Abstract

Understanding the relationship between the composition of the human gut microbiota and the ecological forces shaping it is of great importance; however, knowledge of the biogeographical and ecological relationships between physically interacting taxa is limited. Interbacterial antagonism may play an important role in gut community dynamics, yet the conditions under which antagonistic behaviour is favoured or disfavoured by selection in the gut are not well understood. Here, using genomics, we show that a species-specific type VI secretion system (T6SS) repeatedly acquires inactivating mutations in Bacteroides fragilis in the human gut. This result implies a fitness cost to the T6SS, but we could not identify laboratory conditions under which such a cost manifests. Strikingly, experiments in mice illustrate that the T6SS can be favoured or disfavoured in the gut depending on the strains and species in the surrounding community and their susceptibility to T6SS antagonism. We use ecological modelling to explore the conditions that could underlie these results and find that community spatial structure modulates interaction patterns among bacteria, thereby modulating the costs and benefits of T6SS activity. Our findings point towards new integrative models for interrogating the evolutionary dynamics of type VI secretion and other modes of antagonistic interaction in microbiomes.

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Fig. 1: The GA3 T6SS is associated with altered composition of the human gut microbiota.
Fig. 2: Recurrent evolutionary loss of the GA3 T6SS from B. fragilis.
Fig. 3: Mouse colonization reveals a fitness cost of the B. fragilis GA3 T6SS.
Fig. 4: Cocolonization with a sensitive strain alters producer–resistant strain dynamics in mice.
Fig. 5: Reaction–diffusion model reveals local and spatial dynamics of T6SS producer, resistant and sensitive genotypes.
Fig. 6: Individual-based biofilm simulations suggest dispersal-recolonization regimes can dictate selective loss of T6SS.

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Data availability

The amplicon sequencing data generated in this study are publicly available through the Sequence Read Archive at the National Center for Biotechnology Information (NCBI) under BioProject accession number PRJNA986820. Source data are provided with this paper.

Code availability

Detailed analysis scripts are available at https://github.com/BenRossLab/T6SS-Loss.

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Acknowledgements

We thank the members of Dartmouth College Joint Evolutionary Microbiology Meeting and Microbiology and Microbial Pathogenesis (M2P2) communities and J. Mougous for feedback on this work. We also thank N. Pudlo and E. Martens for technical advice, BENEO for providing Synergy inulin, H. Bernstein for anti-TssD and A. Goodman for providing B. fragilis strains and plasmids. This work was supported by start-up funding from Dartmouth College Geisel School of Medicine and NIH grants R00GM129874 and R35GM142685 to B.D.R.; NSF grant IOS 2017879, Simons Foundation award no. 826672 and HFSP award number RGY0077/2020 to C.D.N.; NIH P20 GM130454 to D.S.; and the Dartmouth College BioMT Core funded by P20GM113132.

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Authors and Affiliations

  1. Department of Microbiology and Immunology, Geisel School of Medicine at Dartmouth College, Hanover, NH, USA

    Sophie Robitaille, Adrian J. Verster, Emily Ann McClure, Darlene B. Royce, Evan Trus, Kerry Swartz, Daniel Schultz & Benjamin D. Ross

  2. Department of Biological Sciences, Dartmouth College, Hanover, NH, USA

    Emilia L. Simmons & Carey D. Nadell

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Contributions

B.D.R., C.D.N. and D.S. conceived of this work. S.R., E.L.S., A.J.V., D.S., E.A.M. and D.B.R. developed the methodology. S.R., E.L.S., A.J.V., E.A.M., D.B.R., E.T., K.S. and D.S. undertook the investigation. S.R., E.L.S., A.J.V., E.A.M. and D.S. produced the visualization. B.D.R., D.S. and C.D.N. were responsible for supervision. B.D.R., S.R., A.J.V., C.D.N. and D.S. wrote the original draft and B.D.R., S.R., E.L.S., A.J.V., E.A.M., D.S. and C.D.N. were involved in reviewing and editing the final manuscript.

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Correspondence to Benjamin D. Ross.

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Extended data

Extended Data Fig. 1 Abrogation of T6SS activity does not provide a fitness benefit to B. fragilis under laboratory conditions growing on mono and di-saccharide as carbon source.

Growth curves and solid growth in mono and coculture for the producer and resistant strains subjected to growth on different sole carbon sources (mono and di-saccharide) in defined minimal broth or solid agar media, including D-fructose (a), D-galactose (b), D-xylose (c) and sucrose (d). For solid agar growth coculture, producer and resistant strains were mixed at a 1:1 ratio by OD600, inoculated in high-density spots before being harvested for enumeration of colony-forming units by plating on BHIS supplemented with either erythromycin or tetracycline. Two-sided Mann-Whitney tests at each timepoint indicated no significant difference between strains. For liquid experiments, the results are from three biological replicates that each represent the mean of eight technical replicates. For solid growth, results are from six biological replicates from two independent experiments. Data shown represent mean values ± SD.

Source data

Extended Data Fig. 2 Abrogation of T6SS activity does not provide a fitness benefit to B. fragilis under laboratory conditions growing on polysaccharides as carbon source.

The growth of the producer and resistant strains in defined minimal media with different carbon sources (polysaccharide) is shown in liquid and solid (mono and coculture) growth in the different panels. For solid growth, B. fragilis producer strain with ErmR and resistant strain with TetR were grown on defined minimal media with different carbon sources separately (monoculture) and together in a 1:1 ratio (coculture). Each strain was quantified via calculating colony-forming units on BHIS agar plates supplemented with erythromycin or tetracycline. Carbon sources used in defined minimal media included potato starch (a), glycogen (b) and mucin (c). Two-sided Mann-Whitney tests showed no difference between the different strains at each timepoint. For liquid experiments, the results are from three biological replicates that each represent the mean of eight technical replicates. For solid growth, results are from six biological replicates from two independent experiments. Data shown represent mean values ± SD.

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Robitaille, S., Simmons, E.L., Verster, A.J. et al. Community composition and the environment modulate the population dynamics of type VI secretion in human gut bacteria. Nat Ecol Evol 7, 2092–2107 (2023). https://doi.org/10.1038/s41559-023-02230-6

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  • DOI: https://doi.org/10.1038/s41559-023-02230-6

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