Shaping a bacterial genome by large chromosomal replacements, the evolutionary history of Streptococcus agalactiae

Abstract

Bacterial populations are subject to complex processes of diversification that involve mutation and horizontal DNA transfer mediated by transformation, transduction, or conjugation. Tracing the evolutionary events leading to genetic changes allows us to infer the history of a microbe. Here, we combine experimental and in silico approaches to explore the forces that drive the genome dynamics of Streptococcus agalactiae, the leading cause of neonatal infections. We demonstrate that large DNA segments of up to 334 kb of the chromosome of S. agalactiae can be transferred through conjugation from multiple initiation sites. Consistently, a genome-wide map analysis of nucleotide polymorphisms among eight human isolates demonstrated that each chromosome is a mosaic of large chromosomal fragments from different ancestors suggesting that large DNA exchanges have contributed to the genome dynamics in the natural population. The analysis of the resulting genetic flux led us to propose a model for the evolutionary history of this species in which clonal complexes of clinical importance derived from a single clone that evolved by exchanging large chromosomal regions with more distantly related strains. The emergence of this clone could be linked to selective sweeps associated with the reduction of genetic diversity in three regions within a large panel of human isolates. Up to now sex in bacteria has been assumed to involve mainly small regions; our results define S. agalactiae as an alternative paradigm in the study of bacterial evolution.

Sequence type 1 group B Streptococcus , an emerging cause of invasive disease in adults, evolves by small genetic changes

“…Moreover, diversity in the ST-1 strains was primarily driven by small genetic events rather than recombination. This finding was somewhat unexpected, as recombination has been found to be a major driver of GBS genetic diversity when diverse serotypes are analyzed (3,10). Together with previous studies, these data suggest that GBS evolution may be viewed as similar to the antigenic shift/antigenic drift model of influenza in which recombination drives the emergence of new GBS subtypes (as may have occurred for serotype V in the mid1970s), which then slowly accumulate new genetic polymorphisms over time.…”

“…This genetic variation can have profound impact on host-pathogen interaction by affecting transmissibility, infection severity, and antimicrobial resistance (2,5,6). The observed genetic intraspecies variability can arise via many distinct mechanisms including large-scale events such as recombination and bacteriophage-mediated horizontal gene transfer as well as small-scale genetic changes such as short insertions, deletions, and/or single nucleotide changes (2,3,5).…”

“…A major outcome of the rapid expansion of available bacterial genomes has been the appreciation of the marked intraspecies genetic variability present in a wide variety of human bacterial pathogens (3,4). This genetic variation can have profound impact on host-pathogen interaction by affecting transmissibility, infection severity, and antimicrobial resistance (2,5,6).…”

Key experimental evidence of chromosomal DNA transfer among selected tuberculosis-causing mycobacteria

“…Conjugation is besides transformation and transduction one of the three principal processes how bacteria may exchange DNA, thereby representing an important accelerator for evolution and adaptation to new environments (14,15,30). For mycobacteria, in contrast to other bacterial genera, knowledge about HGT processes remains scarce.…”

Physiological impact of transposable elements encoding DDE transposases in the environmental adaptation of Streptococcus agalactiae

“…TnGBS2 was also reported to promote the conjugative transfer of chromosomal DNA (Brochet et al, 2008b).…”