Rapid molecular evolution of Spiroplasma symbionts of Drosophila



Gerth, Michael, Martinez-Montoya, Humberto, Ramirez, Paulino, Masson, Florent, Griffin, Joanne S ORCID: 0000-0002-6401-7544, Aramayo, Rodolfo, Siozios, Stefanos ORCID: 0000-0002-1104-7061, Lemaitre, Bruno, Mateos, Mariana and Hurst, Gregory DD ORCID: 0000-0002-7163-7784
(2021) Rapid molecular evolution of Spiroplasma symbionts of Drosophila. MICROBIAL GENOMICS, 7 (2). pp. 1-15.

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Abstract

<i>Spiroplasma</i> is a genus of <i>Mollicutes</i> whose members include plant pathogens, insect pathogens and endosymbionts of animals. <i>Spiroplasma</i> phenotypes have been repeatedly observed to be spontaneously lost in <i>Drosophila</i> cultures, and several studies have documented a high genomic turnover in <i>Spiroplasma</i> symbionts and plant pathogens. These observations suggest that <i>Spiroplasma</i> evolves quickly in comparison to other insect symbionts. Here, we systematically assess evolutionary rates and patterns of <i>Spiroplasma poulsonii</i>, a natural symbiont of <i>Drosophila</i>. We analysed genomic evolution of <i>s</i>Hy within flies, and <i>s</i>Mel within <i>in vitro</i> culture over several years. We observed that <i>S. poulsonii</i> substitution rates are among the highest reported for any bacteria, and around two orders of magnitude higher compared with other inherited arthropod endosymbionts. The absence of mismatch repair loci <i>mutS</i> and <i>mutL</i> is conserved across <i>Spiroplasma</i>, and likely contributes to elevated substitution rates. Further, the closely related strains <i>s</i>Mel and <i>s</i>Hy (>99.5 % sequence identity in shared loci) show extensive structural genomic differences, which potentially indicates a higher degree of host adaptation in <i>s</i>Hy, a protective symbiont of <i>Drosophila hydei</i>. Finally, comparison across diverse <i>Spiroplasma</i> lineages confirms previous reports of dynamic evolution of toxins, and identifies loci similar to the male-killing toxin Spaid in several <i>Spiroplasma</i> lineages and other endosymbionts. Overall, our results highlight the peculiar nature of <i>Spiroplasma</i> genome evolution, which may explain unusual features of its evolutionary ecology.

Item Type: Article
Uncontrolled Keywords: *Correspondence, mgerth@brookes, ac, uk DNA repair, genome evolution, genome reduction, mycoplasma, symbiosis
Depositing User: Symplectic Admin
Date Deposited: 24 Feb 2021 16:52
Last Modified: 29 Dec 2023 00:55
DOI: 10.1099/mgen.0.000503
Open Access URL: https://doi.org/10.1099/mgen.0.000503
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URI: https://livrepository.liverpool.ac.uk/id/eprint/3115873