Pangenome Analysis of Burkholderia pseudomallei: Genome Evolution Preserves Gene Order despite High Recombination Rates

PLoS One. 2015 Oct 20;10(10):e0140274. doi: 10.1371/journal.pone.0140274. eCollection 2015.

Abstract

The pangenomic diversity in Burkholderia pseudomallei is high, with approximately 5.8% of the genome consisting of genomic islands. Genomic islands are known hotspots for recombination driven primarily by site-specific recombination associated with tRNAs. However, recombination rates in other portions of the genome are also high, a feature we expected to disrupt gene order. We analyzed the pangenome of 37 isolates of B. pseudomallei and demonstrate that the pangenome is 'open', with approximately 136 new genes identified with each new genome sequenced, and that the global core genome consists of 4568±16 homologs. Genes associated with metabolism were statistically overrepresented in the core genome, and genes associated with mobile elements, disease, and motility were primarily associated with accessory portions of the pangenome. The frequency distribution of genes present in between 1 and 37 of the genomes analyzed matches well with a model of genome evolution in which 96% of the genome has very low recombination rates but 4% of the genome recombines readily. Using homologous genes among pairs of genomes, we found that gene order was highly conserved among strains, despite the high recombination rates previously observed. High rates of gene transfer and recombination are incompatible with retaining gene order unless these processes are either highly localized to specific sites within the genome, or are characterized by symmetrical gene gain and loss. Our results demonstrate that both processes occur: localized recombination introduces many new genes at relatively few sites, and recombination throughout the genome generates the novel multi-locus sequence types previously observed while preserving gene order.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Algorithms
  • Burkholderia pseudomallei / classification
  • Burkholderia pseudomallei / genetics*
  • Burkholderia pseudomallei / isolation & purification
  • Evolution, Molecular
  • Gene Order*
  • Gene Transfer, Horizontal
  • Genes, Bacterial / genetics*
  • Genetic Variation
  • Genome, Bacterial / genetics*
  • Models, Genetic
  • Recombination, Genetic
  • Species Specificity

Grants and funding

This work was funded by the US Department of Homeland Security contract no. HSHQDC-10-C-00149 to AT and by the US Defense Threat Reduction Agency under project #CB2847 to HSG and CNR. This report does not represent official policy of the US Government or any of its agencies. This report has been cleared for public release. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.