Genomic acquisition of a capsular polysaccharide virulence cluster by non-pathogenic Burkholderia isolates.
BACKGROUND: Burkholderia thailandensis is a non-pathogenic environmental saprophyte closely related to Burkholderia pseudomallei, the causative agent of the often fatal animal and human disease melioidosis. To study B. thailandensis genomic variation, we profiled 50 isolates using a pan-genome micr...
Main Authors: | , , , , , , , , , , , , , , , , , , , |
---|---|
Format: | Journal article |
Language: | English |
Published: |
2010
|
_version_ | 1797092186699857920 |
---|---|
author | Sim, B Chantratita, N Ooi, W Nandi, T Tewhey, R Wuthiekanun, V Thaipadungpanit, J Tumapa, S Ariyaratne, P Sung, W Sem, X Chua, H Ramnarayanan, K Lin, C Liu, Y Feil, E Glass, M Tan, G Peacock, S Tan, P |
author_facet | Sim, B Chantratita, N Ooi, W Nandi, T Tewhey, R Wuthiekanun, V Thaipadungpanit, J Tumapa, S Ariyaratne, P Sung, W Sem, X Chua, H Ramnarayanan, K Lin, C Liu, Y Feil, E Glass, M Tan, G Peacock, S Tan, P |
author_sort | Sim, B |
collection | OXFORD |
description | BACKGROUND: Burkholderia thailandensis is a non-pathogenic environmental saprophyte closely related to Burkholderia pseudomallei, the causative agent of the often fatal animal and human disease melioidosis. To study B. thailandensis genomic variation, we profiled 50 isolates using a pan-genome microarray comprising genomic elements from 28 Burkholderia strains and species. RESULTS: Of 39 genomic regions variably present across the B. thailandensis strains, 13 regions corresponded to known genomic islands, while 26 regions were novel. Variant B. thailandensis isolates exhibited isolated acquisition of a capsular polysaccharide biosynthesis gene cluster (B. pseudomallei-like capsular polysaccharide) closely resembling a similar cluster in B. pseudomallei that is essential for virulence in mammals; presence of this cluster was confirmed by whole genome sequencing of a representative variant strain (B. thailandensis E555). Both whole-genome microarray and multi-locus sequence typing analysis revealed that the variant strains formed part of a phylogenetic subgroup distinct from the ancestral B. thailandensis population and were associated with atypical isolation sources when compared to the majority of previously described B. thailandensis strains. In functional assays, B. thailandensis E555 exhibited several B. pseudomallei-like phenotypes, including colony wrinkling, resistance to human complement binding, and intracellular macrophage survival. However, in murine infection assays, B. thailandensis E555 did not exhibit enhanced virulence relative to other B. thailandensis strains, suggesting that additional factors are required to successfully colonize and infect mammals. CONCLUSIONS: The discovery of such novel variant strains demonstrates how unbiased genomic surveys of non-pathogenic isolates can reveal insights into the development and emergence of new pathogenic species. |
first_indexed | 2024-03-07T03:42:34Z |
format | Journal article |
id | oxford-uuid:be6720bf-0ebd-432c-99e8-fb85680a7ace |
institution | University of Oxford |
language | English |
last_indexed | 2024-03-07T03:42:34Z |
publishDate | 2010 |
record_format | dspace |
spelling | oxford-uuid:be6720bf-0ebd-432c-99e8-fb85680a7ace2022-03-27T05:39:10ZGenomic acquisition of a capsular polysaccharide virulence cluster by non-pathogenic Burkholderia isolates.Journal articlehttp://purl.org/coar/resource_type/c_dcae04bcuuid:be6720bf-0ebd-432c-99e8-fb85680a7aceEnglishSymplectic Elements at Oxford2010Sim, BChantratita, NOoi, WNandi, TTewhey, RWuthiekanun, VThaipadungpanit, JTumapa, SAriyaratne, PSung, WSem, XChua, HRamnarayanan, KLin, CLiu, YFeil, EGlass, MTan, GPeacock, STan, P BACKGROUND: Burkholderia thailandensis is a non-pathogenic environmental saprophyte closely related to Burkholderia pseudomallei, the causative agent of the often fatal animal and human disease melioidosis. To study B. thailandensis genomic variation, we profiled 50 isolates using a pan-genome microarray comprising genomic elements from 28 Burkholderia strains and species. RESULTS: Of 39 genomic regions variably present across the B. thailandensis strains, 13 regions corresponded to known genomic islands, while 26 regions were novel. Variant B. thailandensis isolates exhibited isolated acquisition of a capsular polysaccharide biosynthesis gene cluster (B. pseudomallei-like capsular polysaccharide) closely resembling a similar cluster in B. pseudomallei that is essential for virulence in mammals; presence of this cluster was confirmed by whole genome sequencing of a representative variant strain (B. thailandensis E555). Both whole-genome microarray and multi-locus sequence typing analysis revealed that the variant strains formed part of a phylogenetic subgroup distinct from the ancestral B. thailandensis population and were associated with atypical isolation sources when compared to the majority of previously described B. thailandensis strains. In functional assays, B. thailandensis E555 exhibited several B. pseudomallei-like phenotypes, including colony wrinkling, resistance to human complement binding, and intracellular macrophage survival. However, in murine infection assays, B. thailandensis E555 did not exhibit enhanced virulence relative to other B. thailandensis strains, suggesting that additional factors are required to successfully colonize and infect mammals. CONCLUSIONS: The discovery of such novel variant strains demonstrates how unbiased genomic surveys of non-pathogenic isolates can reveal insights into the development and emergence of new pathogenic species. |
spellingShingle | Sim, B Chantratita, N Ooi, W Nandi, T Tewhey, R Wuthiekanun, V Thaipadungpanit, J Tumapa, S Ariyaratne, P Sung, W Sem, X Chua, H Ramnarayanan, K Lin, C Liu, Y Feil, E Glass, M Tan, G Peacock, S Tan, P Genomic acquisition of a capsular polysaccharide virulence cluster by non-pathogenic Burkholderia isolates. |
title | Genomic acquisition of a capsular polysaccharide virulence cluster by non-pathogenic Burkholderia isolates. |
title_full | Genomic acquisition of a capsular polysaccharide virulence cluster by non-pathogenic Burkholderia isolates. |
title_fullStr | Genomic acquisition of a capsular polysaccharide virulence cluster by non-pathogenic Burkholderia isolates. |
title_full_unstemmed | Genomic acquisition of a capsular polysaccharide virulence cluster by non-pathogenic Burkholderia isolates. |
title_short | Genomic acquisition of a capsular polysaccharide virulence cluster by non-pathogenic Burkholderia isolates. |
title_sort | genomic acquisition of a capsular polysaccharide virulence cluster by non pathogenic burkholderia isolates |
work_keys_str_mv | AT simb genomicacquisitionofacapsularpolysaccharidevirulenceclusterbynonpathogenicburkholderiaisolates AT chantratitan genomicacquisitionofacapsularpolysaccharidevirulenceclusterbynonpathogenicburkholderiaisolates AT ooiw genomicacquisitionofacapsularpolysaccharidevirulenceclusterbynonpathogenicburkholderiaisolates AT nandit genomicacquisitionofacapsularpolysaccharidevirulenceclusterbynonpathogenicburkholderiaisolates AT tewheyr genomicacquisitionofacapsularpolysaccharidevirulenceclusterbynonpathogenicburkholderiaisolates AT wuthiekanunv genomicacquisitionofacapsularpolysaccharidevirulenceclusterbynonpathogenicburkholderiaisolates AT thaipadungpanitj genomicacquisitionofacapsularpolysaccharidevirulenceclusterbynonpathogenicburkholderiaisolates AT tumapas genomicacquisitionofacapsularpolysaccharidevirulenceclusterbynonpathogenicburkholderiaisolates AT ariyaratnep genomicacquisitionofacapsularpolysaccharidevirulenceclusterbynonpathogenicburkholderiaisolates AT sungw genomicacquisitionofacapsularpolysaccharidevirulenceclusterbynonpathogenicburkholderiaisolates AT semx genomicacquisitionofacapsularpolysaccharidevirulenceclusterbynonpathogenicburkholderiaisolates AT chuah genomicacquisitionofacapsularpolysaccharidevirulenceclusterbynonpathogenicburkholderiaisolates AT ramnarayanank genomicacquisitionofacapsularpolysaccharidevirulenceclusterbynonpathogenicburkholderiaisolates AT linc genomicacquisitionofacapsularpolysaccharidevirulenceclusterbynonpathogenicburkholderiaisolates AT liuy genomicacquisitionofacapsularpolysaccharidevirulenceclusterbynonpathogenicburkholderiaisolates AT feile genomicacquisitionofacapsularpolysaccharidevirulenceclusterbynonpathogenicburkholderiaisolates AT glassm genomicacquisitionofacapsularpolysaccharidevirulenceclusterbynonpathogenicburkholderiaisolates AT tang genomicacquisitionofacapsularpolysaccharidevirulenceclusterbynonpathogenicburkholderiaisolates AT peacocks genomicacquisitionofacapsularpolysaccharidevirulenceclusterbynonpathogenicburkholderiaisolates AT tanp genomicacquisitionofacapsularpolysaccharidevirulenceclusterbynonpathogenicburkholderiaisolates |