Reductive evolution in Streptococcus agalactiae and the emergence of a host adapted lineage

Background: During host specialization, inactivation of genes whose function is no more required is favored by changes in selective constraints and evolutionary bottlenecks. The Gram positive bacteria Streptococcus agalactiae (also called GBS), responsible for septicemia and meningitis in neonates also emerged during the seventies as a cause of severe epidemics in fish farms. To decipher the genetic basis for the emergence of these highly virulent GBS strains and of their adaptation to fish, we have analyzed the genomic sequence of seven strains isolated from fish and other poikilotherms. Results: Comparative analysis shows that the two groups of GBS strains responsible for fish epidemic diseases are only distantly related. While strains belonging to the clonal complex 7 cannot be distinguished from their human CC7 counterparts according to their gene content, strains belonging to the ST260-261 types probably diverged a long time ago. In this lineage, specialization to the fish host was correlated with a massive gene inactivation and broad changes in gene expression. We took advantage of the low level of sequence divergence between GBS strains and of the emergence of sublineages to reconstruct the different steps involved in this process. Non-homologous recombination was found to have played a major role in the genome erosion. Conclusions: Our results show that the early phase of genome reduction during host specialization mostly involves accumulation of small and likely reversible indels, followed by a second evolutionary step marked by a higher frequency of large deletions.