Barriers to genetic exchange between bacterial species: Streptococcus pneumoniae transformation

Abstract

Interspecies genetic exchange is an important evolutionary mechanism in bacteria. It allows rapid acquisition of novel functions by transmission of adaptive genes between related species. However, the frequency of homologous recombination between bacterial species decreases sharply with the extent of DNA sequence divergence between the donor and the recipient. In Bacillus and Escherichia, this sexual isolation has been shown to be an exponential function of sequence divergence. Here we demonstrate that sexual isolation in transformation between Streptococcus pneumoniae recipient strains and donor DNA from related strains and species follows the described exponential relationship. We show that the Hex mismatch repair system poses a significant barrier to recombination over the entire range of sequence divergence (0.6 to 27%) investigated. Although mismatch repair becomes partially saturated, it is responsible for 34% of the observed sexual isolation. This is greater than the role of mismatch repair in Bacillus but less than that in Escherichia. The remaining non-Hex-mediated barrier to recombination can be provided by a variety of mechanisms. We discuss the possible additional mechanisms of sexual isolation, in view of earlier findings from Bacillus, Escherichia, and Streptococcus.

FIG. 1

Phylogeny of S. pneumoniae and related species, based on 1,380 bases of the rpoB sequence. The tree is the single most parsimonious phylogeny, created using the exhaustive search algorithm of PAUP, version 3.1.1 (D. L. Swofford, PAUP. Phylogenetic analysis using parsimony, version 4, Sinauer Associates, Sunderland, Mass., 1998). Branching confidence values are based on 1,000 bootstrap replicates. DNA sequence divergences between each donor strain and the S. pneumoniae recipients are shown on the right. The above phylogeny agrees with results obtained by analysis of 16S rRNA and sodA genes, with the notable exception that S. anginosus clusters here with S. constellatus, whereas earlier results show it to be more closely related to S. intermedius. The high bootstrap confidence value of this grouping suggests a possible recombination event at rpoB.

FIG. 2

Log₁₀ (sexual isolation) versus sequence divergence between each donor and recipient. Sexual isolation values were calculated by dividing the frequency of homogamic recombination (using the donor's own Rif^r DNA) by the frequency of heterogamic recombination (using a divergent donor's DNA). The sexual isolation shown for the wild-type recipients is the average value for the two wild-type recipient strains, Pn16 and R6. The sexual isolation in the absence of mismatch repair is the result of transformation of the R6Δ3 hexA mutant. φ_wt and φ_Hex⁻ are the slopes of the regression of log₁₀ (sexual isolation) on sequence divergence for the wild type and the Hex⁻ mutant, respectively.