Reductive genome evolution from the mother of Rickettsia

Guillaume Blanc, Hiroyuki Ogata, Catherine Robert, Stéphane Audic, Karsten Suhre, Guy Vestris, Jean Michel Claverie, Didier Raoult

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Abstract

The Rickettsia genus is a group of obligate intracellular α-proteobacteria representing a paradigm of reductive evolution. Here, we investigate the evolutionary processes that shaped the genomes of the genus. The reconstruction of ancestral genomes indicates that their last common ancestor contained more genes, but already possessed most traits associated with cellular parasitism. The differences in gene repertoires across modern Rickettsia are mainly the result of differential gene losses from the ancestor. We demonstrate using computer simulation that the propensity of loss was variable across genes during this process. We also analyzed the ratio of nonsynonymous to synonymous changes (Ka/Ks) calculated as an average over large sets of genes to assay the strength of selection acting on the genomes of Rickettsia, Anaplasmataceae, and free-living γ-proteobacteria. As a general trend, Ka/Ks were found to decrease with increasing divergence between genomes. The high Ka/Ks for closely related genomes are probably due to a lag in the removal of slightly deleterious nonsynonymous mutations by natural selection. Interestingly, we also observed a decrease of the rate of gene loss with increasing divergence, suggesting a similar lag in the removal of slightly deleterious pseudogene alleles. For larger divergence (Ks > 0.2), Ka/Ks converge toward similar values indicating that the levels of selection are roughly equivalent between intracellular α-proteobacteria and their free-living relatives. This contrasts with the view that obligate endocellular microorganisms tend to evolve faster as a consequence of reduced effectiveness of selection, and suggests a major role of enhanced background mutation rates on the fast protein divergence in the obligate intracellular α-proteobacteria.

Original languageEnglish
Pages (from-to)103-114
Number of pages12
JournalPLoS genetics
Volume3
Issue number1
DOIs
Publication statusPublished - 1 Jan 2007

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ASJC Scopus subject areas

  • Ecology, Evolution, Behavior and Systematics
  • Molecular Biology
  • Genetics
  • Genetics(clinical)
  • Cancer Research

Cite this

Blanc, G., Ogata, H., Robert, C., Audic, S., Suhre, K., Vestris, G., Claverie, J. M., & Raoult, D. (2007). Reductive genome evolution from the mother of Rickettsia. PLoS genetics, 3(1), 103-114. https://doi.org/10.1371/journal.pgen.0030014