Article

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

  • Nature Ecology & Evolution 111601167 (2017)
  • doi:10.1038/s41559-017-0237-0
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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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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.

Author information

Author notes

    • Denis H. Lynn

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

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.

Competing interests

The authors declare no competing financial interests.

Corresponding author

Correspondence to Patrick J. Keeling.

Electronic supplementary material

  1. Supplementary Information

    Supplementary Figures 1–7 and Supplementary Discussion

  2. Supplementary Data 1

    Functional modules

  3. Supplementary Data 2

    dS and dN/dS comparisons