Genomic analysis of the multi-host pathogen Erysipelothrix rhusiopathiae reveals extensive recombination as well as the existence of three generalist clades with wide geographic distribution

Abstract

BackgroundKnowledge about how bacterial populations are structured is an important prerequisite for studying their ecology and evolutionary history and facilitates inquiry into host specificity, pathogenicity, geographic dispersal and molecular epidemiology. Erysipelothrix rhusiopathiae is an opportunistic pathogen that is currently reemerging in both the swine and poultry industries globally. This bacterium sporadically causes mortalities in captive marine mammals, and has recently been implicated in large-scale wildlife die-offs. However, despite its economic relevance and broad geographic and host distribution, including zoonotic potential, the global diversity, recombination rates, and population structure of this bacterium remain poorly characterized. In this study, we conducted a broad-scale genomic comparison of E. rhusiopathiae based on a diverse collection of isolates in order to address these knowledge gaps.ResultsEighty-three E. rhusiopathiae isolates from a range of host species and geographic origins, isolated between 1958 and 2014, were sequenced and assembled using both reference-based mapping and de novo assembly. We found that a high proportion of the core genome (58 %) had undergone recombination. Therefore, we used three independent methods robust to the presence of recombination to define the population structure of this species: a phylogenetic tree based on a set of conserved protein sequences, in silico chromosome painting, and network analysis. All three methods were broadly concordant and supported the existence of three distinct clades within the species E. rhusiopathiae. Although we found some evidence of host and geographical clustering, each clade included isolates from diverse host species and from multiple continents.ConclusionsUsing whole genome sequence data, we confirm recent suggestions that E. rhusiopathiae is a weakly clonal species that has been shaped extensively by homologous recombination. Despite frequent recombination, we can reliably identify three distinct clades that do not clearly segregate by host species or geographic origin. Our results provide an essential baseline for future molecular epidemiological, ecological and evolutionary studies of E. rhusiopathiae and facilitate comparisons to other recombinogenic, multi-host bacteria.Electronic supplementary materialThe online version of this article (doi:10.1186/s12864-016-2643-0) contains supplementary material, which is available to authorized users.

Clonal Lineages of Erysipelothrix rhusiopathiae Responsible for Acute Swine Erysipelas in Japan Identified by Using Genome-Wide Single-Nucleotide Polymorphism Analysis

“…The results of this study also showed no clear correlations between the geographic origins or years of isolation of the strains and the PFGE patterns. This may be because of chromosomal rearrangements resulting from a high level of core genome recombination among E. rhusiopathiae strains (16). It is also possible that the serovar 1a strains analyzed in this study are not phylogenetically related because of homoplasy in serotype (16).…”

“…In each analyzed strain, Ͼ95.6% of the Illumina reads (mostly Ͼ99%) were mapped to the reference genome, and the mapped regions covered Ͼ98.0% (mostly Ͼ99%) of the reference genome (Table S1). A recent study clarified the existence of three distinct clades (clades 1, 2, and 3) and an "intermediate" clade between clade 2 and the dominant clade 3 within the species E. rhusiopathiae (16). To examine the phylogenetic position of the Japanese strains, we constructed a phylogenetic tree by including the strains belonging to clades 2 and 3 and the two recently sequenced Chinese strains, SY1027 and GXBY-1, both of which were isolated from septicemic pigs (17,18).…”

“…To examine the phylogenetic position of the Japanese strains, we constructed a phylogenetic tree by including the strains belonging to clades 2 and 3 and the two recently sequenced Chinese strains, SY1027 and GXBY-1, both of which were isolated from septicemic pigs (17,18). In that study, the Fujisawa and SY1027 strains were found to belong to the intermediate clade (16).…”

“…This may be because of chromosomal rearrangements resulting from a high level of core genome recombination among E. rhusiopathiae strains (16). It is also possible that the serovar 1a strains analyzed in this study are not phylogenetically related because of homoplasy in serotype (16). Thus, the PFGE-based genotyping provided little information regarding the genetic relatedness between the recent Japanese isolates and older isolates or the vaccine strain; therefore, we next performed spaA genotyping.…”

“…To further investigate the genetic relatedness among the strains, we employed a high-resolution genotyping method, i.e., genome-wide SNP analysis of these clinical isolates. Recently, using whole-genome sequence data from 83 E. rhusiopathiae isolates from a wide range of hosts and geographic origins, Forde et al revealed that E. rhusiopathiae consists of three distinct clades that are not clearly segregated by host species or geographic origin (16). The authors showed that isolates in clade 1 exclusively contained a single copy of the surface-protective antigen type B gene (spaB), while all other isolates among the two other clades (clades 2 and 3) had a single copy of the spaA gene.…”