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.

Figure 1

Phylogenetic tree of 16S rRNA genes from eubacteria and mitochondria: Buchnera (Buchnera sp.); E. coli, Haemophilus (Haemophilus influenzae), Neisseria (Neisseria meningitidis), protist mt (R. americana mt), plant mt (Arabidopsis thaliana mt), Rickettsia (Rickettsia prowazekii), Bacillus (Bacillus subtilis), and Mycobacterium (Mycobacterium tuberculosis). We used 1,358 nucleotides, excluding gap sites. The proteobacterial portion of the tree was rooted by using Gram-positive bacteria. This tree was reconstructed by the neighbor-joining method with the Tamura–Nei-γ distance (12, 13). A γ parameter was estimated to be 0.665 by Gu and Zhang's method (14). Numbers besides branches indicate percent bootstrap values with 1,000 replications.

Figure 2

Branch lengths of orthologous proteins between (a) E. coli and Buchnera sp. and (b) R. prowazekii and the mt of R. americana. Closed circles indicate the proteins involved in amino acid biosynthesis in Buchnera and those involved in respiration and ATP synthesis in the mt, respectively. Triangles are proteins in all other functional categories. The abscissa and the ordinate represent the number of amino acid replacements per site.