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Parallel genome reduction in symbionts descended from closely related free-living bacteria

Nature Ecology & Evolution volume 1, pages 1160–1167 (2017)Cite this article

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Abstract

Endosymbiosis plays an important role in ecology and evolution, but fundamental aspects of the origin of intracellular symbionts remain unclear. The extreme age of many symbiotic relationships, lack of data on free-living ancestors and uniqueness of each event hinder investigations. Here, we describe multiple strains of the bacterium Polynucleobacter that evolved independently and under similar conditions from closely related, free-living ancestors to become obligate endosymbionts of closely related ciliate hosts. As these genomes reduced in parallel from similar starting states, they provide unique glimpses into the mechanisms underlying genome reduction in symbionts. We found that gene loss is contingently lineage-specific, with no evidence for ordered streamlining. However, some genes in otherwise disrupted pathways are retained, possibly reflecting cryptic genetic network complexity. We also measured substitution rates between many endosymbiotic and free-living pairs for hundreds of genes, which showed that genetic drift, and not mutation pressure, is the main non-selective factor driving molecular evolution in endosymbionts.

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Figure 1: Genomic reduction in symbiotic Polynucleobacter strains.
Figure 2: Phylogenomic tree of symbiotic and free-living Polynucleobacter.
Figure 3: Protein-coding genes shared by symbiotic Polynucleobacter strains.
Figure 4: Examples of within-module gene losses in symbiotic Polynucleobacter.
Figure 5: Pairwise comparisons of dS and dN/dS values.

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Change history

  • 27 February 2018

    The Supplementary Information file originally published with this Article was missing Supplementary Figs 1–7. This has now been corrected.

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Acknowledgements

We thank S. Gabrielli for helping with the artwork. This work was supported by grants from the Natural Sciences and Engineering Research Council of Canada (227301 and 6544-2013 awarded to P.J.K. and D.H.L, respectively). V.B. and M.K. were supported by fellowships from the Tula Foundation to the Centre for Microbial Diversity and Evolution.

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Author notes

  1. Denis H. Lynn

    Present address: Department of Zoology, University of British Columbia, Vancouver, BC, V6T 1Z4, Canada

Authors and Affiliations

  1. Department of Botany, University of British Columbia, Vancouver, BC, V6T 1Z4, Canada

    Vittorio Boscaro, Martin Kolisko & Patrick J. Keeling

  2. Department of Biology, University of Pisa, Pisa, 56126, Italy

    Vittorio Boscaro & Claudia Vannini

  3. Institute of Parasitology, Biology Centre, Czech Academy of Sciences, Prague, 370 05, Czech Republic

    Martin Kolisko

  4. Department of Chemistry, University of Konstanz, Konstanz, 78464, Germany

    Michele Felletti

  5. Department of Integrative Biology, University of Guelph, Guelph, ON, N1G 2W1, Canada

    Denis H. Lynn

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Contributions

V.B., D.H.L. and P.J.K. designed the study. V.B. sampled and isolated the ciliates. V.B. and C.V. cultured, screened and identified the Euplotes strains and Polynucleobacter symbionts. C.V. performed the isolation experiments on the symbionts. V.B. and C.V. optimized and performed the genomic DNA extractions. D.H.L. prepared the libraries. V.B. assembled and annotated the genomes. V.B. and M.F. conducted the functional analysis. M.K. performed the phylogenomic inference, clustering analysis and dN/dS calculations. V.B., M.K. and P.J.K. wrote the paper. All authors participated in the drafting process.

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Correspondence to Patrick J. Keeling.

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A correction to this article is available online at https://doi.org/10.1038/s41559-018-0484-8.

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Supplementary Information

Supplementary Figures 1–7 and Supplementary Discussion

Supplementary Data 1

Functional modules

Supplementary Data 2

dS and dN/dS comparisons

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Boscaro, V., Kolisko, M., Felletti, M. et al. Parallel genome reduction in symbionts descended from closely related free-living bacteria. Nat Ecol Evol 1, 1160–1167 (2017). https://doi.org/10.1038/s41559-017-0237-0

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