Trends in prokaryotic evolution revealed by comparison of closely related bacterial and archaeal genomes - PubMed (original) (raw)

Pavel S Novichkov et al. J Bacteriol. 2009 Jan.

Abstract

In order to explore microevolutionary trends in bacteria and archaea, we constructed a data set of 41 alignable tight genome clusters (ATGCs). We show that the ratio of the medians of nonsynonymous to synonymous substitution rates (dN/dS) that is used as a measure of the purifying selection pressure on protein sequences is a stable characteristic of the ATGCs. In agreement with previous findings, parasitic bacteria, notwithstanding the sometimes dramatic genome shrinkage caused by gene loss, are typically subjected to relatively weak purifying selection, presumably owing to relatively small effective population sizes and frequent bottlenecks. However, no evidence of genome streamlining caused by strong selective pressure was found in any of the ATGCs. On the contrary, a significant positive correlation between the genome size, as well as gene size, and selective pressure was observed, although a variety of free-living prokaryotes with very close selective pressures span nearly the entire range of genome sizes. In addition, we examined the connections between the sequence evolution rate and other genomic features. Although gene order changes much faster than protein sequences during the evolution of prokaryotes, a strong positive correlation was observed between the "rearrangement distance" and the amino acid distance, suggesting that at least some of the events leading to genome rearrangement are subjected to the same type of selective constraints as the evolution of amino acid sequences.

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Figures

FIG. 1.

FIG. 1.

Distributions of dS, dN, and dN/dS in orthologous gene sets from three genome pairs from different ATGCs. (a) Distribution (probability density) of dN. (b) Distribution (probability density) of dS. (c) Distribution (probability density) of dN/dS. Metma, Methanococcus maripaludis C5-M. maripaludis C7 (Euryarchaeota); Bursp, Burkholderia cenocepacia MC0-3-Burkholderia vietnamiensis G4 (Betaproteobacteria); Salsp, Salinispora arenicola CNS-205-Salinispora tropica CNB-440 (Actinobacteria). The distribution curves were obtained by Gaussian-kernel smoothing of the individual data points (28).

FIG. 2.

FIG. 2.

Dependence of DN/DS on the distance between genomes, measured as DN. Each point corresponds to a pair of genomes in the given ATGC. (a) Xanthomonas sp. (b) Shewanella sp. (c) P. marinus.

FIG. 3.

FIG. 3.

Distribution (probability density) of DN/DS in the 41 analyzed ATGCs. The distribution curve was obtained by Gaussian-kernel smoothing of the individual data points (28).

FIG. 4.

FIG. 4.

Correlations between the purifying selection pressure (DN/DS) and other genomic variables. (a) DN/DS versus genome size. (b) DN/DS versus intergenic-region size. (c) DN/DS versus gene density. (d) DN/DS versus protein-coding-gene size. The dashed lines show linear regressions. Rs, Spearman ranking correlation coefficient.

FIG. 5.

FIG. 5.

PCA of seven genomic variables. (a) Loadings of the first two PCs. (b) Scatter of the ATGCs in the plane of the first two PCs. The red contour encloses the tight cluster of genomes, mostly those of free-living organisms, that are subjeced to relatively strong purifying selection. The three ATGCs that include various strains of P. marinus are denoted Pm.

FIG. 6.

FIG. 6.

Patterns of genome rearrangement in prokaryotes. (a) Nearly complete decay of synteny (DY = 0.69; DN = 0.15; DS ≫ 1); Streptococcus sanguinis SK36 and Streptococcus pneumoniae R6. (b) Virtual absence of rearrangement (DY ∼ 0; DN = 0.06; DS = 1.12); Chlamydophila caviae GPIC and Chlamydophila abortus S26/3. (c) Multiple inversions with limited transposition of individual genes (DY ∼ 0; DN = 0; DS = 0); Yersinia pestis Antiqua and Y. pestis CO92. (d) No inversion; hot spots of transposition of individual genes (DY = 0.04; DN = 0.03; DS = 0.41); P. marinus AS9601 and P. marinus MIT 9215. (e) Multiple inversions and transposition of individual genes (DY = 0.16; DN = 0.08; DS = 1.35); Pseudomonas fluorescens PfO-1 and P. fluorescens Pf-5.

FIG. 7.

FIG. 7.

Correlation between the mean purifying selection pressures affecting amino acid sequence evolution (DN/DS) and genome rearrangement (DY/DS). Rs, Spearman ranking correlation coefficient.

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