Phylogenomics and the dynamic genome evolution of the genus Streptococcus

Abstract

The genus Streptococcus comprises important pathogens that have a severe impact on human health and are responsible for substantial economic losses to agriculture. Here, we utilize 46 Streptococcus genome sequences (44 species), including eight species sequenced here, to provide the first genomic level insight into the evolutionary history and genetic basis underlying the functional diversity of all major groups of this genus. Gene gain/loss analysis revealed a dynamic pattern of genome evolution characterized by an initial period of gene gain followed by a period of loss, as the major groups within the genus diversified. This was followed by a period of genome expansion associated with the origins of the present extant species. The pattern is concordant with an emerging view that genomes evolve through a dynamic process of expansion and streamlining. A large proportion of the pan-genome has experienced lateral gene transfer (LGT) with causative factors, such as relatedness and shared environment, operating over different evolutionary scales. Multiple gene ontology terms were significantly enriched for each group, and mapping terms onto the phylogeny showed that those corresponding to genes born on branches leading to the major groups represented approximately one-fifth of those enriched. Furthermore, despite the extensive LGT, several biochemical characteristics have been retained since group formation, suggesting genomic cohesiveness through time, and that these characteristics may be fundamental to each group. For example, proteolysis: mitis group; urea metabolism: salivarius group; carbohydrate metabolism: pyogenic group; and transcription regulation: bovis group.

Keywords: comparative genomics; enrichment; gene gain and loss; lateral gene transfer; phylogenetics.

Fig. 1.—

Phylogenies derived from a core set of 136 genes. Left: Consensus of the phylogenetic signal from each gene (numbers on branches show the proportion of genes that support a particular grouping). Right: ML phylogeny derived from a concatenation of the genes (numbers on branches show bootstrap support). Each of the major eight groups is color shaded. The putative downei group is shown with a dashed line. Previous nomenclature for species within the bovis group is shown within parentheses.

Fig. 2.—

Result of gene gain/loss analysis. Boxes on nodes and tips of the phylogeny show genome size (genome size calculations exclude one MCL gene cluster that was excluded from the analysis—see Materials and Methods). Numbers on branches show the number of gains, losses, and the overall balance (gain–loss: balance), with red indicating an overall gain and blue an overall loss. Color shading for each major Streptococcus group follows figure 1.

Fig. 3.—

Hierarchal clustering among genomes using presence/absence of MCL gene clusters. Approximately unbiased P values are shown on branches. Color shading for each major Streptococcus group follows figure 1.