Comparative genomics of the bacterial genus Streptococcus illuminates evolutionary implications of species groups.

Xiao-Yang Gao,Xiao-Yang Zhi,Wen-Jun Li,Hans-Peter Klenk,Hong-Wei Li,Sean D Reid

doi:10.1371/journal.pone.0101229

Abstract

Members of the genus Streptococcus within the phylum Firmicutes are among the most diverse and significant zoonotic pathogens. This genus has gone through considerable taxonomic revision due to increasing improvements of chemotaxonomic approaches, DNA hybridization and 16S rRNA gene sequencing. It is proposed to place the majority of streptococci into “species groups”. However, the evolutionary implications of species groups are not clear presently. We use comparative genomic approaches to yield a better understanding of the evolution of Streptococcus through genome dynamics, population structure, phylogenies and virulence factor distribution of species groups. Genome dynamics analyses indicate that the pan-genome size increases with the addition of newly sequenced strains, while the core genome size decreases with sequential addition at the genus level and species group level. Population structure analysis reveals two distinct lineages, one including Pyogenic, Bovis, Mutans and Salivarius groups, and the other including Mitis, Anginosus and Unknown groups. Phylogenetic dendrograms show that species within the same species group cluster together, and infer two main clades in accordance with population structure analysis. Distribution of streptococcal virulence factors has no obvious patterns among the species groups; however, the evolution of some common virulence factors is congruous with the evolution of species groups, according to phylogenetic inference. We suggest that the proposed streptococcal species groups are reasonable from the viewpoints of comparative genomics; evolution of the genus is congruent with the individual evolutionary trajectories of different species groups.

Highlights

The genus Streptococcus comprises a wide variety of pathogenic and commensal gram-positive bacteria [1]
The analyses enabled us to test (1) pan-genome size and core genome size of Streptococcus and species groups; (2) the phylogenetic relationships among those groups based on genomic data; (3) the reasonableness of species groups raised by associated biochemical features and 16S rRNA gene analysis; and (4) distribution of virulence factor among species groups, in order to explore their implications in evolution of the genus
Applications of chemotaxonomic approaches, DNA hybridization and 16S rRNA gene sequencing have resulted in the proposal of ‘‘species groups’’ for streptococci with various lifestyles

Summary

Introduction

The genus Streptococcus comprises a wide variety of pathogenic and commensal gram-positive bacteria [1]. Recent applications of chemotaxonomic approaches, genomic DNA-DNA hybridization and 16S rRNA sequencing techniques have provided significant insights into the natural relationships among streptococci, but have influenced significantly their taxonomy and nomenclature [10,11,12,13] These revisions form the basis of delineation and reveal the natural grouping of species into ‘‘species groups’’ [14]. The species groups have been named ‘‘Pyogenic’’, ‘‘Mitis’’, ‘‘Anginosus’’, ‘‘Bovis’’, ‘‘Mutans’’ and ‘‘Salivarius’’ respectively, and they encompass the majority of described species (several species remain ungrouped) These polyphasic taxonomy approaches are still widely used in many laboratories, limits of biochemical determination, and low efficiency operation of DNA hybridization [15] as well as possible phenotypic and ecological differentiation underlying identical 16S rRNA genes [16] all inevitably hamper the evolutionary and taxonomic investigations of streptococci.

Methods

Results

Conclusion