Purifying selection and molecular adaptation in the genome of Verminephrobacter, the heritable symbiotic bacteria of earthworms

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  • Kasper U Kjeldsen
  • Thomas Bataillon
  • Nicolás Pinel, Department of Civil and Environmental Engineering, University of Washington , United States
  • Stéphane De Mita, Institut de Recherche pour le Développement, France
  • Marie B Lund, Denmark
  • Frank Panitz
  • Christian Bendixen, Denmark
  • David A Stahl, Department of Civil and Environmental Engineering, University of Washington , United States
  • Andreas Schramm
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 MYA) association with earthworms. We assembled a draft genome of Verminephrobacter aporrectodeae and compared it to the genomes of Verminephrobacter eiseniae and two non-symbiotic 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 to 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 bi-parental transmission of symbionts and rare genetic mixing during transmission can prevent genome erosion in heritable symbionts.
Original languageEnglish
JournalGenome Biology and Evolution
Volume4
Issue3
Pages (from-to)307-315
Number of pages9
ISSN1759-6653
DOIs
Publication statusPublished - 2012

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