Purifying Selection and Molecular Adaptation in the Genome of Verminephrobacter, the Heritable Symbiotic Bacteria of Earthworms

Kasper U. Kjeldsen; Thomas Bataillon; Nicolás Pinel; Stéphane De Mita; Marie B. Lund; Frank Panitz; Christian Bendixen; David A. Stahl; Andreas Schramm

doi:10.1093/gbe/evs014

Article de revue

Purifying Selection and Molecular Adaptation in the Genome of Verminephrobacter, the Heritable Symbiotic Bacteria of Earthworms

Kasper U. Kjeldsen, Thomas Bataillon, Nicolás Pinel, Stéphane De Mita, Marie B. Lund, Frank Panitz, Christian Bendixen, David A. Stahl et Andreas Schramm

Genome biology and evolution, Vol.4(3), pp.307-315

01/01/2012

DOI: https://doi.org/10.1093/gbe/evs014

PMID: 22333491

Résumé

Letters

While genomic erosion is common among intracellular symbionts, patterns of genome evolution in heritable extracellular endosymbionts remain elusive. We study vertically transmitted extracellular endosymbionts (Verminephrobacter, Betaproteobacteria) that form a beneficial, species-specific, and evolutionarily old (60–130 Myr) association with earthworms. We assembled a draft genome of Verminephrobacter aporrectodeae and compared it with the genomes of Verminephrobacter eiseniae and two nonsymbiotic close relatives (Acidovorax). Similar to V. eiseniae, the V. aporrectodeae genome was not markedly reduced in size and showed no A–T bias. We characterized the strength of purifying selection (ω = dN/dS) and codon usage bias in 876 orthologous genes. Symbiont genomes exhibited strong purifying selection (ω = 0.09 ± 0.07), although transition to symbiosis entailed relaxation of purifying selection as evidenced by 50% higher ω values and less codon usage bias in symbiont compared with reference genomes. Relaxation was not evenly distributed among functional gene categories but was overrepresented in genes involved in signal transduction and cell envelope biogenesis. The same gene categories also harbored instances of positive selection in the Verminephrobacter clade. In total, positive selection was detected in 89 genes, including also genes involved in DNA metabolism, tRNA modification, and TonB-dependent iron uptake, potentially highlighting functions important in symbiosis. Our results suggest that the transition to symbiosis was accompanied by molecular adaptation, while purifying selection was only moderately relaxed, despite the evolutionary age and stability of the host association. We hypothesize that biparental transmission of symbionts and rare genetic mixing during transmission can prevent genome erosion in heritable symbionts.

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Détails

Titre: Purifying Selection and Molecular Adaptation in the Genome of Verminephrobacter, the Heritable Symbiotic Bacteria of Earthworms
Créateurs - sans rôle: Kasper U. Kjeldsen - Department of Bioscience, Microbiology, Aarhus University, Denmark Center for Geomicrobiology, Department of Bioscience, Aarhus University, Denmark Bioinformatics Research Center, Aarhus University, Denmark Department of Civil and Environmental Engineering, University of Washington Institut de Recherche pour le Développement, Montpellier, France Department of Molecular Biology and Genetics, Aarhus University, Tjele, Denmark
Thomas Bataillon - Department of Bioscience, Microbiology, Aarhus University, Denmark Center for Geomicrobiology, Department of Bioscience, Aarhus University, Denmark Bioinformatics Research Center, Aarhus University, Denmark Department of Civil and Environmental Engineering, University of Washington Institut de Recherche pour le Développement, Montpellier, France Department of Molecular Biology and Genetics, Aarhus University, Tjele, Denmark
Nicolás Pinel - Department of Bioscience, Microbiology, Aarhus University, Denmark Center for Geomicrobiology, Department of Bioscience, Aarhus University, Denmark Bioinformatics Research Center, Aarhus University, Denmark Department of Civil and Environmental Engineering, University of Washington Institut de Recherche pour le Développement, Montpellier, France Department of Molecular Biology and Genetics, Aarhus University, Tjele, Denmark
Stéphane De Mita - Department of Bioscience, Microbiology, Aarhus University, Denmark Center for Geomicrobiology, Department of Bioscience, Aarhus University, Denmark Bioinformatics Research Center, Aarhus University, Denmark Department of Civil and Environmental Engineering, University of Washington Institut de Recherche pour le Développement, Montpellier, France Department of Molecular Biology and Genetics, Aarhus University, Tjele, Denmark
Marie B. Lund - Department of Bioscience, Microbiology, Aarhus University, Denmark Center for Geomicrobiology, Department of Bioscience, Aarhus University, Denmark Bioinformatics Research Center, Aarhus University, Denmark Department of Civil and Environmental Engineering, University of Washington Institut de Recherche pour le Développement, Montpellier, France Department of Molecular Biology and Genetics, Aarhus University, Tjele, Denmark
Frank Panitz - Department of Bioscience, Microbiology, Aarhus University, Denmark Center for Geomicrobiology, Department of Bioscience, Aarhus University, Denmark Bioinformatics Research Center, Aarhus University, Denmark Department of Civil and Environmental Engineering, University of Washington Institut de Recherche pour le Développement, Montpellier, France Department of Molecular Biology and Genetics, Aarhus University, Tjele, Denmark
Christian Bendixen - Department of Bioscience, Microbiology, Aarhus University, Denmark Center for Geomicrobiology, Department of Bioscience, Aarhus University, Denmark Bioinformatics Research Center, Aarhus University, Denmark Department of Civil and Environmental Engineering, University of Washington Institut de Recherche pour le Développement, Montpellier, France Department of Molecular Biology and Genetics, Aarhus University, Tjele, Denmark
David A. Stahl - Department of Bioscience, Microbiology, Aarhus University, Denmark Center for Geomicrobiology, Department of Bioscience, Aarhus University, Denmark Bioinformatics Research Center, Aarhus University, Denmark Department of Civil and Environmental Engineering, University of Washington Institut de Recherche pour le Développement, Montpellier, France Department of Molecular Biology and Genetics, Aarhus University, Tjele, Denmark
Andreas Schramm - Department of Bioscience, Microbiology, Aarhus University, Denmark Center for Geomicrobiology, Department of Bioscience, Aarhus University, Denmark Bioinformatics Research Center, Aarhus University, Denmark Department of Civil and Environmental Engineering, University of Washington Institut de Recherche pour le Développement, Montpellier, France Department of Molecular Biology and Genetics, Aarhus University, Tjele, Denmark
Détails de publication: Genome biology and evolution, Vol.4(3), pp.307-315
Éditeur: Oxford University Press
Nombre de pages: 9
Identifiants: 99148148509311
Unité académique: Plant Health Institute of Montpellier - PHIM
Langue: English
Type de ressource: Journal article