Pangenome analysis of burkholderia pseudomallei

Genome evolution preserves gene order despite high recombination rates

Senanu M. Spring-Pearson, Joshua K. Stone, Adina Doyle, Christopher J. Allender, Richard T. Okinaka, Mark Mayo, Stacey M. Broomall, Jessica M. Hill, Mark A. Karavis, Kyle S. Hubbard, Joseph M. Insalaco, Lauren A. McNew, C. Nicole Rosenzweig, Henry S. Gibbons, Bart J. Currie, David M Wagner, Paul S Keim, Apichai Tuanyok

Research output: Contribution to journalArticle

10 Citations (Scopus)

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.

Original languageEnglish (US)
Article number140274
JournalPLoS One
Volume10
Issue number10
DOIs
StatePublished - Oct 20 2015

Fingerprint

Burkholderia pseudomallei
Gene Order
Genetic Recombination
preserves
Genes
Genome
genome
genes
genomic islands
Genomic Islands
site-specific recombination
Transfer RNA
gene transfer
Gene Frequency

ASJC Scopus subject areas

  • Agricultural and Biological Sciences(all)
  • Biochemistry, Genetics and Molecular Biology(all)
  • Medicine(all)

Cite this

Spring-Pearson, S. M., Stone, J. K., Doyle, A., Allender, C. J., Okinaka, R. T., Mayo, M., ... Tuanyok, A. (2015). Pangenome analysis of burkholderia pseudomallei: Genome evolution preserves gene order despite high recombination rates. PLoS One, 10(10), [140274]. https://doi.org/10.1371/journal.pone.0140274

Pangenome analysis of burkholderia pseudomallei : Genome evolution preserves gene order despite high recombination rates. / Spring-Pearson, Senanu M.; Stone, Joshua K.; Doyle, Adina; Allender, Christopher J.; Okinaka, Richard T.; Mayo, Mark; Broomall, Stacey M.; Hill, Jessica M.; Karavis, Mark A.; Hubbard, Kyle S.; Insalaco, Joseph M.; McNew, Lauren A.; Rosenzweig, C. Nicole; Gibbons, Henry S.; Currie, Bart J.; Wagner, David M; Keim, Paul S; Tuanyok, Apichai.

In: PLoS One, Vol. 10, No. 10, 140274, 20.10.2015.

Research output: Contribution to journalArticle

Spring-Pearson, SM, Stone, JK, Doyle, A, Allender, CJ, Okinaka, RT, Mayo, M, Broomall, SM, Hill, JM, Karavis, MA, Hubbard, KS, Insalaco, JM, McNew, LA, Rosenzweig, CN, Gibbons, HS, Currie, BJ, Wagner, DM, Keim, PS & Tuanyok, A 2015, 'Pangenome analysis of burkholderia pseudomallei: Genome evolution preserves gene order despite high recombination rates', PLoS One, vol. 10, no. 10, 140274. https://doi.org/10.1371/journal.pone.0140274
Spring-Pearson, Senanu M. ; Stone, Joshua K. ; Doyle, Adina ; Allender, Christopher J. ; Okinaka, Richard T. ; Mayo, Mark ; Broomall, Stacey M. ; Hill, Jessica M. ; Karavis, Mark A. ; Hubbard, Kyle S. ; Insalaco, Joseph M. ; McNew, Lauren A. ; Rosenzweig, C. Nicole ; Gibbons, Henry S. ; Currie, Bart J. ; Wagner, David M ; Keim, Paul S ; Tuanyok, Apichai. / Pangenome analysis of burkholderia pseudomallei : Genome evolution preserves gene order despite high recombination rates. In: PLoS One. 2015 ; Vol. 10, No. 10.
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