Acceleration of genomic evolution caused by enhanced mutation rate in endocellular symbionts

Abstract

Endosymbionts, which are widely observed in nature, have undergone reductive genome evolution because of their long-term intracellular lifestyle. Here we compared the complete genome sequences of two different endosymbionts, Buchnera and a protist mitochondrion, with their close relatives to study the evolutionary rates of functional genes in endosymbionts. The results indicate that the rate of amino acid substitution is two times higher in symbionts than in their relatives. This rate increase was observed uniformly among different functional classes of genes, although strong purifying selection may have counterbalanced the rate increase in a few cases. Our data suggest that, contrary to current views, neither the Muller's ratchet effect nor the slightly deleterious mutation theory sufficiently accounts for the elevated evolutionary rate. Rather, the elevated evolutionary rate appears to be mainly due to enhanced mutation rate, although the possibility of relaxation of purifying selection cannot be ruled out. E ubacteria that live within eukaryotic cells-endocellular symbionts-obtain metabolic precursors synthesized by their hosts and have lost many genes for biosynthetic pathways relative to their free-living cousins (1, 2). Such genome reduction is manifested in Buchnera sp. APS (3, 4), a maternally transmitted obligate ␥-proteobacterial endosymbiont of aphids. This endosymbiont produces essential amino acids for its insect host, which in turn provides nonessential amino acids and other metabolites for the bacterium (1). More extreme genome reduction is observed in mitochondria (2), ATP-producing eukaryotic organelles that stem from endosymbiotic eubacteria and that have relinquished their genome entirely in their anaerobic forms, hydrogenosomes (5).In addition, the rate of amino acid substitution of functional genes is often higher in endosymbionts than in their sister species or bacteria that are considered to be closest to their ancestral species (6-10). This accelerated rate of evolution in endosymbionts is generally believed to occur by Muller's ratchet effect (see below) or by fixation of slightly deleterious mutations in small endosymbiont populations (6-10). However, the acceleration of evolutionary rate may also be caused by a high mutation rate or relaxation of purifying selection in endosymbionts. To distinguish between these two types of hypotheses, we conducted genomic comparison of the endosymbionts Buchnera sp. APS and Reclinomonas americana mitochondrion (mt) with their closest relatives Escherichia coli and Rickettsia prowazekii, respectively, and estimated the relative rates of amino acid substitution for different groups of proteins. Materials and MethodsIdentification of Orthologs. To compare rates of amino acid substitution in endocellular symbionts and relatives, we identified orthologous genes, that is, the genes that were neither duplicated before the divergence of species under study nor horizontally transferred subsequently. We first compared the genome of Buchnera sp. APS with that o...

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