Abstract
BackgroundThe genus Streptococcus comprises pathogens that strongly influence the health of humans and animals. Genome sequencing of multiple Streptococcus strains demonstrated high variability in gene content and order even in closely related strains of the same species and created a newly emerged object for genomic analysis, the pan-genome. Here we analysed the genome evolution of 25 strains of Streptococcus suis, 50 strains of Streptococcus pyogenes and 28 strains of Streptococcus pneumoniae.ResultsFractions of the pan-genome, unique, periphery, and universal genes differ in size, functional composition, the level of nucleotide substitutions, and predisposition to horizontal gene transfer and genomic rearrangements. The density of substitutions in intergenic regions appears to be correlated with selection acting on adjacent genes, implying that more conserved genes tend to have more conserved regulatory regions.The total pan-genome of the genus is open, but only due to strain-specific genes, whereas other pan-genome fractions reach saturation. We have identified the set of genes with phylogenies inconsistent with species and non-conserved location in the chromosome; these genes are rare in at least one species and have likely experienced recent horizontal transfer between species. The strain-specific fraction is enriched with mobile elements and hypothetical proteins, but also contains a number of candidate virulence-related genes, so it may have a strong impact on adaptability and pathogenicity.Mapping the rearrangements to the phylogenetic tree revealed large parallel inversions in all species. A parallel inversion of length 15 kB with breakpoints formed by genes encoding surface antigen proteins PhtD and PhtB in S. pneumoniae leads to replacement of gene fragments that likely indicates the action of an antigen variation mechanism.ConclusionsMembers of genus Streptococcus have a highly dynamic, open pan-genome, that potentially confers them with the ability to adapt to changing environmental conditions, i.e. antibiotic resistance or transmission between different hosts. Hence, integrated analysis of all aspects of genome evolution is important for the identification of potential pathogens and design of drugs and vaccines.
Highlights
The genus Streptococcus comprises pathogens that strongly influence the health of humans and animals
Prediction of virulence-related orthologous groups We found virulence-related genes with MP3 [28] that combined a support vector machine classifier trained on virulence factors from MvirDB [29] and a hidden Markov model classifier based on Pfam domains present in virulence factors
The core genome of studied Streptococcus species is enriched with information-process and main metabolic functions and depleted with mobile elements and phage-related genes; the periphery fraction is enriched with nichespecific metabolic functions, including pathogenesisrelated ones; and strain-specific genes are enriched with hypothetical genes and mobile elements, and contain many virulence-related genes
Summary
The genus Streptococcus comprises pathogens that strongly influence the health of humans and animals. Genome sequencing of multiple Streptococcus strains demonstrated high variability in gene content and order even in closely related strains of the same species and created a newly emerged object for genomic analysis, the pan-genome. The genus Streptococcus are Gram-positive bacteria that exert strong influence on the health of humans and animals. Streptococcus pyogenes is among the top ten of bacterial causes of human mortality worldwide [2, 3], and due to the molecular mimicry with heart and brain cells causes severe autoimmune sequelae like rheumatic fever [4] and, possibly, autoimmune neuropsychiatric disorders [5]. Sequencing of multiple strains of one species has demonstrated that the genome of any single strain does not reflect the genetic variability of the species, as two strains may differ by 20–35% of the gene content [7]. The pan-genome is said to be open if upon addition of new strains its size continues to grow, or closed, if at some point it saturates [7]
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