Purifying selection in mitochondria, free-living and obligate intracellular proteobacteria

The effectiveness of elimination of slightly deleterious mutations depends mainly on drift and recombination frequency. Here we analyze the influence of these two factors on the strength of the purifying selection in mitochondrial and proteobacterial orthologous genes taking into account the differences in the organism lifestyles.

(I) We found that the probability of fixation of nonsynonymous substitutions (Kn/Ks) in mitochondria is significantly lower compared to obligate intracellular bacteria and even marginally significantly lower compared to free-living bacteria. The comparison of bacteria of different lifestyles demonstrates more effective elimination of slightly deleterious mutations in (II) free-living bacteria as compared to obligate intracellular species and in (III) obligate intracellular parasites as compared to obligate intracellular symbionts. (IV) Finally, we observed that the level of the purifying selection (i.e. 1-Kn/Ks) increases with the density of mobile elements in bacterial genomes.

This study shows that the comparison of patterns of molecular evolution of orthologous genes between ecologically different groups of organisms allow to elucidate the genetic consequences of their various lifestyles. Comparing the strength of the purifying selection among proteobacteria with different lifestyles we obtained results, which are in concordance with theoretical expectations: (II) low effective population size and level of recombination in obligate intracellular proteobacteria lead to less effective elimination of mutations compared to free-living relatives; (III) rare horizontal transmissions, i.e. effectively zero recombination level in symbiotic obligate intracellular bacteria leads to less effective purifying selection than in parasitic obligate intracellular bacteria; (IV) the increased frequency of recombination in bacterial genomes with high mobile element density leads to a more effective elimination of slightly deleterious mutations. At the same time, (I) more effective purifying selection in relatively small populations of nonrecombining mitochondria as compared to large populations of recombining proteobacteria was unexpected. We hypothesize that additional features such as the high number of protein-protein interactions or female germ-cell atresia increase evolutionary constraints and maintain the effective purifying selection in mitochondria, but more work is needed to definitely establish these additional features.