A Population Genetics-Based and Phylogenetic Approach to Understanding the Evolution of Virulence in the GenusListeria

Abstract

ABSTRACTThe genusListeriaincludes (i) the opportunistic pathogensL. monocytogenesandL. ivanovii, (ii) the saprotrophsL. innocua,L. marthii, andL. welshimeri, and (iii)L. seeligeri, an apparent saprotroph that nevertheless typically contains theprfAvirulence gene cluster. A novel 10-loci multilocus sequence typing scheme was developed and used to characterize 67 isolates representing sixListeriaspp. (excludingL. grayi) in order to (i) provide an improved understanding of the phylogeny and evolution of the genusListeriaand (ii) useListeriaas a model to study the evolution of pathogenicity in opportunistic environmental pathogens. Phylogenetic analyses identified six well-supportedListeriaspecies that group into two main subdivisions, with each subdivision containing strains with and without theprfAvirulence gene cluster. Stochastic character mapping and phylogenetic analysis ofhly, a gene in theprfAcluster, suggest that the common ancestor of the genusListeriacontained theprfAvirulence gene cluster and that this cluster was lost at least five times during the evolution ofListeria, yielding multiple distinct saprotrophic clades.L. welshimeri, which appears to represent the most ancient clade that arose from an ancestor with aprfAcluster deletion, shows a considerably lower average sequence divergence than otherListeriaspecies, suggesting a population bottleneck and a putatively different ecology than other saprotrophicListeriaspecies. Overall, our data suggest that, for some pathogens, loss of virulence genes may represent a selective advantage, possibly by facilitating adaptation to a specific ecological niche.