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 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.
Department of Biological Sciences, Northern Arizona University, Flagstaff, AZ 86011, United States of America.
Senanu M
SM
Spring-Pearson
Department of Biological Sciences, Northern Arizona University, Flagstaff, AZ 86011, United States of America.
Joshua K
JK
Stone
Department of Biological Sciences, Northern Arizona University, Flagstaff, AZ 86011, United States of America.
Adina
A
Doyle
Department of Biological Sciences, Northern Arizona University, Flagstaff, AZ 86011, United States of America.
Christopher J
CJ
Allender
Department of Biological Sciences, Northern Arizona University, Flagstaff, AZ 86011, United States of America.
Richard T
RT
Okinaka
Menzies School of Health Research and Infectious Disease Department, Royal Darwin Hospital. Darwin, Northern Territory, Australia.
Mark
M
Mayo
BioSciences Division, Edgewood Chemical Biological Center, Aberdeen Proving Ground, MD, United States of America.
Stacey M
SM
Broomall
BioSciences Division, Edgewood Chemical Biological Center, Aberdeen Proving Ground, MD, United States of America.
Jessica M
JM
Hill
BioSciences Division, Edgewood Chemical Biological Center, Aberdeen Proving Ground, MD, United States of America.
Mark A
MA
Karavis
BioSciences Division, Edgewood Chemical Biological Center, Aberdeen Proving Ground, MD, United States of America.
Kyle S
KS
Hubbard
BioSciences Division, Edgewood Chemical Biological Center, Aberdeen Proving Ground, MD, United States of America.
Joseph M
JM
Insalaco
BioSciences Division, Edgewood Chemical Biological Center, Aberdeen Proving Ground, MD, United States of America.
Lauren A
LA
McNew
BioSciences Division, Edgewood Chemical Biological Center, Aberdeen Proving Ground, MD, United States of America.
C Nicole
CN
Rosenzweig
BioSciences Division, Edgewood Chemical Biological Center, Aberdeen Proving Ground, MD, United States of America.
Henry S
HS
Gibbons
Menzies School of Health Research and Infectious Disease Department, Royal Darwin Hospital. Darwin, Northern Territory, Australia.
Bart J
BJ
Currie
Department of Biological Sciences, Northern Arizona University, Flagstaff, AZ 86011, United States of America.
David M
DM
Wagner
Department of Biological Sciences, Northern Arizona University, Flagstaff, AZ 86011, United States of America.
Paul
P
Keim
Department of Biological Sciences, Northern Arizona University, Flagstaff, AZ 86011, United States of America; Department of Infectious Diseases and Pathology, University of Florida, Gainesville, FL, United States of America.
Apichai
A
Tuanyok
D000465:Algorithms; D016957:Burkholderia pseudomallei / Q000145:classification / Q000235:genetics* / Q000302:isolation & purification; D019143:Evolution, Molecular; D023061:Gene Order; D022761:Gene Transfer, Horizontal; D005798:Genes, Bacterial / Q000235:genetics*; D014644:Genetic Variation; D016680:Genome, Bacterial / Q000235:genetics*; D008957:Models, Genetic; D011995:Recombination, Genetic; D013045:Species Specificity