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

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 portio...

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Main Authors: 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 Keim, Apichai Tuanyok
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2015-01-01
Series:PLoS ONE
Online Access:http://europepmc.org/articles/PMC4613141?pdf=render
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spelling doaj-a075fd569677443c86ca413e818c864b2020-11-25T01:56:28ZengPublic Library of Science (PLoS)PLoS ONE1932-62032015-01-011010e014027410.1371/journal.pone.0140274Pangenome Analysis of Burkholderia pseudomallei: Genome Evolution Preserves Gene Order despite High Recombination Rates.Senanu M Spring-PearsonJoshua K StoneAdina DoyleChristopher J AllenderRichard T OkinakaMark MayoStacey M BroomallJessica M HillMark A KaravisKyle S HubbardJoseph M InsalacoLauren A McNewC Nicole RosenzweigHenry S GibbonsBart J CurrieDavid M WagnerPaul KeimApichai TuanyokThe 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.http://europepmc.org/articles/PMC4613141?pdf=render
collection DOAJ
language English
format Article
sources DOAJ
author 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 Keim
Apichai Tuanyok
spellingShingle 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 Keim
Apichai Tuanyok
Pangenome Analysis of Burkholderia pseudomallei: Genome Evolution Preserves Gene Order despite High Recombination Rates.
PLoS ONE
author_facet 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 Keim
Apichai Tuanyok
author_sort Senanu M Spring-Pearson
title Pangenome Analysis of Burkholderia pseudomallei: Genome Evolution Preserves Gene Order despite High Recombination Rates.
title_short Pangenome Analysis of Burkholderia pseudomallei: Genome Evolution Preserves Gene Order despite High Recombination Rates.
title_full Pangenome Analysis of Burkholderia pseudomallei: Genome Evolution Preserves Gene Order despite High Recombination Rates.
title_fullStr Pangenome Analysis of Burkholderia pseudomallei: Genome Evolution Preserves Gene Order despite High Recombination Rates.
title_full_unstemmed Pangenome Analysis of Burkholderia pseudomallei: Genome Evolution Preserves Gene Order despite High Recombination Rates.
title_sort pangenome analysis of burkholderia pseudomallei: genome evolution preserves gene order despite high recombination rates.
publisher Public Library of Science (PLoS)
series PLoS ONE
issn 1932-6203
publishDate 2015-01-01
description 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.
url http://europepmc.org/articles/PMC4613141?pdf=render
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