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Plasmids do not consistently stabilize cooperation across bacteria but may promote broad pathogen host-range

Nature Ecology & Evolution volume 5, pages 1624–1636 (2021)Cite this article

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Abstract

Horizontal gene transfer via plasmids could favour cooperation in bacteria, because transfer of a cooperative gene turns non-cooperative cheats into cooperators. This hypothesis has received support from theoretical, genomic and experimental analyses. By contrast, we show here, with a comparative analysis across 51 diverse species, that genes for extracellular proteins, which are likely to act as cooperative ‘public goods’, were not more likely to be carried on either: (1) plasmids compared to chromosomes; or (2) plasmids that transfer at higher rates. Our results were supported by theoretical modelling which showed that, while horizontal gene transfer can help cooperative genes initially invade a population, it has less influence on the longer-term maintenance of cooperation. Instead, we found that genes for extracellular proteins were more likely to be on plasmids when they coded for pathogenic virulence traits, in pathogenic bacteria with a broad host-range.

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Fig. 1: Three hypotheses about why selection might favour genes coding for extracellular proteins to be located on plasmids.
Fig. 2: Extracellular proteins are not overrepresented on plasmids.
Fig. 3: Plasmid mobility and extracellular proteins.
Fig. 4: Plasmids facilitate the invasion but not the maintenance of cooperation.
Fig. 5: Plasmid loss can favour the maintenance of cooperation.
Fig. 6: Pathogenicity, host-range and the location of genes coding for extracellular proteins.

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Data availability

The dataset of genomes analysed during this study, including PSORTb results and plasmid mobility predictions of MOBsuite, will be made available in the public repository Dryad at: https://doi.org/10.5061/dryad.gxd2547n4

Code availability

Code used to solve equations in the theoretical modelling section of the paper can be found at: https://github.com/ThomasWilliamScott/Plasmid_cooperation.git

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Acknowledgements

We thank C. MacLean, K. Foster, S. Brown, L. Belcher, C. Hao and especially E. Rocha for their helpful comments, and R. Goldberg and V. Pike for their support with MCMCglmm. We thank J. Robertson for providing plasmid mobility data from the MOBsuite database. We thank the BBSRC (BB/M011224/1: A.E.D.), ERC (SESE: J.L.T., A.S.G. and M.G.; 834164: T.W.S and S.A.W.) and NSERC-CRSNG of Canada (G.W.) for funding. Conceptual figures were created with BioRender.com.

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Author notes

  1. These authors contributed equally: Anna E. Dewar, Joshua L. Thomas.

  2. These authors jointly supervised this work: Stuart A. West, Melanie Ghoul.

Authors and Affiliations

  1. Department of Zoology, University of Oxford, Oxford, UK

    Anna E. Dewar, Joshua L. Thomas, Thomas W. Scott, Ashleigh S. Griffin, Stuart A. West & Melanie Ghoul

  2. Department of Applied Mathematics, University of Western Ontario, London, Ontario, Canada

    Geoff Wild

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Contributions

A.E.D., J.L.T., A.S.G., S.A.W. and M.G. conceived the genomic analyses and interpreted results. A.E.D. and J.L.T. collected and analysed the genomic data and A.E.D. produced the corresponding statistical analyses and figures. T.W.S, G.W. and S.A.W. conceived the theoretical modelling and interpreted results. T.W.S. completed the formal theoretical modelling. A.E.D., J.L.T., T.W.S., S.A.W. and M.G. wrote and/or edited the manuscript. A.E.D. wrote and put together Supplementary Sections 1, 2 and 3 and T.W.S. wrote and put together Supplementary Section 4. All authors commented on and approved the manuscript for submission.

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Correspondence to Anna E. Dewar.

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The authors declare no competing interests.

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

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Extended data

Extended Data Fig. 1 Protein subcellular localizations.

Visualization of all possible subcellular locations predicted by PSORTb. The left panel shows a cross-section of a typical Gram-negative bacterium and the right panel shows the equivalent for a Gram-positive bacterium. Both kinds of bacteria have an inner membrane, known as the cytoplasmic membrane. The main difference is that Gram-positive bacteria are surrounded by a thick layer of a molecule called peptidoglycan, while Gram-negative bacteria have a much thinner layer of peptidoglycan, and have an additional membrane. Created with BioRender.com.

Extended Data Fig. 2 Substantial variation within and between species in the genomic location of extracellular proteins.

The x-axis is the % of genomes in each species where the proportion of plasmid proteins predicted as extracellular is greater than the proportion of chromosome proteins predicted as extracellular. Crucially, this considers only whether the plasmid proportion is greater than the chromosome proportion for each genome, rather than also considering the magnitude of the difference (Fig. 2). Error bars are the 95% Confidence Intervals from a binomial test on each species, comparing the number of genomes which have plasmid proportion > chromosome proportion to a null prediction of 50% of genomes. Species in blue have >50% of genomes where plasmid > chromosome extracellular proportion, meaning extracellular proteins are significantly over-represented on plasmids. Species in red have <50% of genomes where plasmid > chromosome extracellular proportion, meaning extracellular proteins are significantly over-represented on chromosomes. Species in grey have a 95% CI which overlaps 50%, so extracellular proteins are not significantly over-represented on either plasmids or chromosomes in these species.

Extended Data Fig. 3 Difference in plasmid and chromosome proportion for all protein classes predicted by PSORTb.

The x-axis is the difference in plasmid and chromosome extracellular proportions, as in Fig. 2. The y-axis is all possible subcellular locations predicted by PSORTb. These protein ‘classes’ are ordered along the y-axis by location within the cell, from intracellular to increasingly extracellular. Each dot is the posterior mean and 95% Credible Intervals from a MCMCglmm42 on the difference in plasmid and chromosome proportion across all species, accounting for phylogeny and sample size. The only proteins significantly over-represented in either direction are unknown proteins, which make up a higher proportion of plasmid proteins in all species we analysed.

Extended Data Fig. 4 No effect of plasmid mobility on the difference in plasmid and chromosome proportion of genes coding for extracellular proteins.

The x-axis is the % of a species’ plasmids which are conjugative or mobilizable. The y-axis shows the difference in the plasmid and chromosome proportions of genes coding for extracellular proteins, as in Fig. 2. Each dot is the mean for all genomes in a species. Species in blue are those with genes coding for extracellular proteins over-represented on plasmids, while species in red have genes coding for extracellular proteins over-represented on chromosomes.

Extended Data Fig. 5 No difference in where extracellular proteins are coded for in pathogens compared to non-pathogens.

The y-axis shows the difference in the plasmid and chromosome proportion of genes coding for extracellular proteins. Each dot is the mean for all genomes in a species. Species in blue are those with genes coding for extracellular proteins over-represented on plasmids, while species in red have genes coding for extracellular proteins over-represented on chromosomes. Species were categorized as pathogens or non-pathogens; those we could not classify as either are shown in the ‘Opportunistic + others’ category. The black bars indicate the mean for all species in each category.

Extended Data Fig. 6 Additional measures of environmental variability.

We used two additional methods to estimate the environmental variability encountered by these species. (a) The x-axis shows published data on the number of five broad environments each species was recorded in, which we supplemented with information from the literature to include all species. (b) The x-axis shows the proportion of each species’ genes which are ‘core’ genes, meaning they are found in all members of the species. The y-axis in both graphs shows the difference in the proportion of genes on plasmids and chromosomes coding for extracellular proteins. Each dot is the mean for all genomes in a species. Species in blue are those with extracellular proteins over-represented on plasmids, while species in red are those with extracellular proteins over-represented on chromosomes. For both these measures, we found no significant correlation with the genomic location of genes coding for extracellular proteins across species.

Supplementary information

Supplementary Information

Supplementary Genomics Results and Discussion (Section 1), Tables 1–3 (Section 2), Figs. 1–10 (Section 3) and Modelling Methods, Results, Discussion and Figs. 11–14 (Section 4).

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Dewar, A.E., Thomas, J.L., Scott, T.W. et al. Plasmids do not consistently stabilize cooperation across bacteria but may promote broad pathogen host-range. Nat Ecol Evol 5, 1624–1636 (2021). https://doi.org/10.1038/s41559-021-01573-2

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