Phenotypic differentiation of Streptococcus pyogenes populations is induced by recombination-driven gene-specific sweeps.
Genomic recombination plays an important role in driving adaptive evolution and population differentiation in bacteria. However, controversy exists as to the effects of recombination on population diversity and differentiation, i.e., recombination is frequent enough to sweep through the population at selected gene loci (gene-specific sweeps), or the recombination rate is low without interfering genome-wide selective sweeps. Observations supporting either view are sparse. Pathogenic bacteria causing infectious diseases are promising candidates to provide observations of recombination. However, phenotype-associated differentiations are usually vague among them due to diverse disease manifestations. Here we report a population genomic study of the group A Streptococcus pyogenes (GAS), a human pathogen with highly recombining genomes. By employing a genome-wide association study on single nucleotide polymorphisms (SNPs), we demonstrate a phenotypic differentiation of GAS, represented by separate clustering of two sublineages associated with niche-specific infections, i.e., skin infection and pharyngitis-induced acute rheumatic fever. By quantifying SNPs associated with the differentiation in a statistical and phylogenetic context, we propose that the phenotype-associated differentiation arose through recombination-driven gene-specific sweeps, rather than genome-wide sweeps. Our work provides a novel paradigm of phenotype-associated differentiation induced by gene-specific sweeps in a human pathogen and has implications for understanding of driving forces of bacterial evolution.
W.M. Keck Center for Transgene Research, University of Notre Dame, Notre Dame, IN 46556, USA.
Yun-Juan
YJ
Bao
Département de Sciences Biologiques, Université de Montréal, Montréal, QC H3C 3J7, Canada.
B Jesse
BJ
Shapiro
W.M. Keck Center for Transgene Research, University of Notre Dame, Notre Dame, IN 46556, USA.|Department of Biological Sciences, University of Notre Dame, Notre Dame, IN 46556, USA.
Shaun W
SW
Lee
W.M. Keck Center for Transgene Research, University of Notre Dame, Notre Dame, IN 46556, USA.|Department of Chemistry and Biochemistry, University of Notre Dame, Notre Dame, IN 46556, USA.
Victoria A
VA
Ploplis
W.M. Keck Center for Transgene Research, University of Notre Dame, Notre Dame, IN 46556, USA.|Department of Chemistry and Biochemistry, University of Notre Dame, Notre Dame, IN 46556, USA.
Francis J
FJ
Castellino
D056426:Genetic Loci; D016680:Genome, Bacterial; D006801:Humans; D020641:Polymorphism, Single Nucleotide; D011995:Recombination, Genetic; D013297:Streptococcus pyogenes / Q000235:genetics*