Abstract

BackgroundPhylogeographic reconstruction of some bacterial populations is hindered by low diversity coupled with high levels of lateral gene transfer. A comparison of recombination levels and diversity at seven housekeeping genes for eleven bacterial species, most of which are commonly cited as having high levels of lateral gene transfer shows that the relative contributions of homologous recombination versus mutation for Burkholderia pseudomallei is over two times higher than for Streptococcus pneumoniae and is thus the highest value yet reported in bacteria. Despite the potential for homologous recombination to increase diversity, B. pseudomallei exhibits a relative lack of diversity at these loci. In these situations, whole genome genotyping of orthologous shared single nucleotide polymorphism loci, discovered using next generation sequencing technologies, can provide very large data sets capable of estimating core phylogenetic relationships. We compared and searched 43 whole genome sequences of B. pseudomallei and its closest relatives for single nucleotide polymorphisms in orthologous shared regions to use in phylogenetic reconstruction.ResultsBayesian phylogenetic analyses of >14,000 single nucleotide polymorphisms yielded completely resolved trees for these 43 strains with high levels of statistical support. These results enable a better understanding of a separate analysis of population differentiation among >1,700 B. pseudomallei isolates as defined by sequence data from seven housekeeping genes. We analyzed this larger data set for population structure and allele sharing that can be attributed to lateral gene transfer. Our results suggest that despite an almost panmictic population, we can detect two distinct populations of B. pseudomallei that conform to biogeographic patterns found in many plant and animal species. That is, separation along Wallace's Line, a biogeographic boundary between Southeast Asia and Australia.ConclusionWe describe an Australian origin for B. pseudomallei, characterized by a single introduction event into Southeast Asia during a recent glacial period, and variable levels of lateral gene transfer within populations. These patterns provide insights into mechanisms of genetic diversification in B. pseudomallei and its closest relatives, and provide a framework for integrating the traditionally separate fields of population genetics and phylogenetics for other bacterial species with high levels of lateral gene transfer.

Highlights

  • Phylogeographic reconstruction of some bacterial populations is hindered by low diversity coupled with high levels of lateral gene transfer

  • The availability of multiple whole genome sequence (WGS) has led to more accurate reconstructions of phylogenetic relationships within several bacterial species [1,2,3,4,5,6,7,8,9], but all of these studies have been limited by a small number of WGSs (19 or fewer genomes)

  • Phylogenetic patterns revealed by shared, orthologous single nucleotide polymorphism (SNP) derived from WGSs Bayesian phylogenetic analysis of 11,208 orthologous SNPs shared among all WGSs confirmed the distant relationship of B. thailandensis and the monophyletic derivation of B. mallei from a B. pseudomallei lineage (Figure 1)

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Summary

Introduction

Phylogeographic reconstruction of some bacterial populations is hindered by low diversity coupled with high levels of lateral gene transfer. Despite the potential for homologous recombination to increase diversity, B. pseudomallei exhibits a relative lack of diversity at these loci In these situations, whole genome genotyping of orthologous shared single nucleotide polymorphism loci, discovered using generation sequencing technologies, can provide very large data sets capable of estimating core phylogenetic relationships. Character differences, as measured by single nucleotide polymorphisms (SNPs), are assumed to have arisen only once in their evolutionary history These two species exhibit no evidence of conspecific lateral gene transfer (LGT), which can cause apparent homoplasy by placing alleles with common origins in different genetic backgrounds. Recent sequencing efforts for B. pseudomallei and other closely related species provided the opportunity for pioneering phylogenetic work on a species with high levels of LGT

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