Cargando…

The Arabinose 5-Phosphate Isomerase KdsD Is Required for Virulence in Burkholderia pseudomallei

Burkholderia pseudomallei is the causative agent of melioidosis, which is endemic primarily in Southeast Asia and northern Australia but is increasingly being seen in other tropical and subtropical regions of the world. Melioidosis is associated with high morbidity and mortality rates, which is medi...

Descripción completa

Detalles Bibliográficos
Autores principales: Jenkins, Christopher H., Scott, Andrew E., O’Neill, Paul A., Norville, Isobel H., Prior, Joann L., Ireland, Philip M.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: American Society for Microbiology 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10448790/
https://www.ncbi.nlm.nih.gov/pubmed/37458584
http://dx.doi.org/10.1128/jb.00034-23
_version_ 1785094810158235648
author Jenkins, Christopher H.
Scott, Andrew E.
O’Neill, Paul A.
Norville, Isobel H.
Prior, Joann L.
Ireland, Philip M.
author_facet Jenkins, Christopher H.
Scott, Andrew E.
O’Neill, Paul A.
Norville, Isobel H.
Prior, Joann L.
Ireland, Philip M.
author_sort Jenkins, Christopher H.
collection PubMed
description Burkholderia pseudomallei is the causative agent of melioidosis, which is endemic primarily in Southeast Asia and northern Australia but is increasingly being seen in other tropical and subtropical regions of the world. Melioidosis is associated with high morbidity and mortality rates, which is mediated by the wide range of virulence factors encoded by B. pseudomallei. These virulence determinants include surface polysaccharides such as lipopolysaccharide (LPS) and capsular polysaccharides (CPS). Here, we investigated a predicted arabinose-5-phosphate isomerase (API) similar to KdsD in B. pseudomallei strain K96243. KdsD is required for the production of the highly conserved 3-deoxy-d-manno-octulosonic acid (Kdo), a key sugar in the core region of LPS. Recombinant KdsD was expressed and purified, and API activity was determined. Although a putative API paralogue (KpsF) is also predicted to be encoded, the deletion of kdsD resulted in growth defects, loss of motility, reduced survival in RAW 264.7 murine macrophages, and attenuation in a BALB/c mouse model of melioidosis. Suppressor mutations were observed during a phenotypic screen for motility, revealing single nucleotide polymorphisms or indels located in the poorly understood CPS type IV cluster. Crucially, suppressor mutations did not result in reversion of attenuation in vivo. This study demonstrates the importance of KdsD for B. pseudomallei virulence and highlights further the complex nature of the polysaccharides it produces. IMPORTANCE The intrinsic resistance of B. pseudomallei to many antibiotics complicates treatment. This opportunistic pathogen possesses a wide range of virulence factors, resulting in severe and potentially fatal disease. Virulence factors as targets for drug development offer an alternative approach to combat pathogenic bacteria. Prior to initiating early drug discovery approaches, it is important to demonstrate that disruption of the target gene will prevent the development of disease. This study highlights the fact that KdsD is crucial for virulence of B. pseudomallei in an animal model of infection and provides supportive phenotypic characterization that builds a foundation for future therapeutic development.
format Online
Article
Text
id pubmed-10448790
institution National Center for Biotechnology Information
language English
publishDate 2023
publisher American Society for Microbiology
record_format MEDLINE/PubMed
spelling pubmed-104487902023-08-25 The Arabinose 5-Phosphate Isomerase KdsD Is Required for Virulence in Burkholderia pseudomallei Jenkins, Christopher H. Scott, Andrew E. O’Neill, Paul A. Norville, Isobel H. Prior, Joann L. Ireland, Philip M. J Bacteriol Research Article Burkholderia pseudomallei is the causative agent of melioidosis, which is endemic primarily in Southeast Asia and northern Australia but is increasingly being seen in other tropical and subtropical regions of the world. Melioidosis is associated with high morbidity and mortality rates, which is mediated by the wide range of virulence factors encoded by B. pseudomallei. These virulence determinants include surface polysaccharides such as lipopolysaccharide (LPS) and capsular polysaccharides (CPS). Here, we investigated a predicted arabinose-5-phosphate isomerase (API) similar to KdsD in B. pseudomallei strain K96243. KdsD is required for the production of the highly conserved 3-deoxy-d-manno-octulosonic acid (Kdo), a key sugar in the core region of LPS. Recombinant KdsD was expressed and purified, and API activity was determined. Although a putative API paralogue (KpsF) is also predicted to be encoded, the deletion of kdsD resulted in growth defects, loss of motility, reduced survival in RAW 264.7 murine macrophages, and attenuation in a BALB/c mouse model of melioidosis. Suppressor mutations were observed during a phenotypic screen for motility, revealing single nucleotide polymorphisms or indels located in the poorly understood CPS type IV cluster. Crucially, suppressor mutations did not result in reversion of attenuation in vivo. This study demonstrates the importance of KdsD for B. pseudomallei virulence and highlights further the complex nature of the polysaccharides it produces. IMPORTANCE The intrinsic resistance of B. pseudomallei to many antibiotics complicates treatment. This opportunistic pathogen possesses a wide range of virulence factors, resulting in severe and potentially fatal disease. Virulence factors as targets for drug development offer an alternative approach to combat pathogenic bacteria. Prior to initiating early drug discovery approaches, it is important to demonstrate that disruption of the target gene will prevent the development of disease. This study highlights the fact that KdsD is crucial for virulence of B. pseudomallei in an animal model of infection and provides supportive phenotypic characterization that builds a foundation for future therapeutic development. American Society for Microbiology 2023-07-17 /pmc/articles/PMC10448790/ /pubmed/37458584 http://dx.doi.org/10.1128/jb.00034-23 Text en © Crown copyright 2023. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Research Article
Jenkins, Christopher H.
Scott, Andrew E.
O’Neill, Paul A.
Norville, Isobel H.
Prior, Joann L.
Ireland, Philip M.
The Arabinose 5-Phosphate Isomerase KdsD Is Required for Virulence in Burkholderia pseudomallei
title The Arabinose 5-Phosphate Isomerase KdsD Is Required for Virulence in Burkholderia pseudomallei
title_full The Arabinose 5-Phosphate Isomerase KdsD Is Required for Virulence in Burkholderia pseudomallei
title_fullStr The Arabinose 5-Phosphate Isomerase KdsD Is Required for Virulence in Burkholderia pseudomallei
title_full_unstemmed The Arabinose 5-Phosphate Isomerase KdsD Is Required for Virulence in Burkholderia pseudomallei
title_short The Arabinose 5-Phosphate Isomerase KdsD Is Required for Virulence in Burkholderia pseudomallei
title_sort arabinose 5-phosphate isomerase kdsd is required for virulence in burkholderia pseudomallei
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10448790/
https://www.ncbi.nlm.nih.gov/pubmed/37458584
http://dx.doi.org/10.1128/jb.00034-23
work_keys_str_mv AT jenkinschristopherh thearabinose5phosphateisomerasekdsdisrequiredforvirulenceinburkholderiapseudomallei
AT scottandrewe thearabinose5phosphateisomerasekdsdisrequiredforvirulenceinburkholderiapseudomallei
AT oneillpaula thearabinose5phosphateisomerasekdsdisrequiredforvirulenceinburkholderiapseudomallei
AT norvilleisobelh thearabinose5phosphateisomerasekdsdisrequiredforvirulenceinburkholderiapseudomallei
AT priorjoannl thearabinose5phosphateisomerasekdsdisrequiredforvirulenceinburkholderiapseudomallei
AT irelandphilipm thearabinose5phosphateisomerasekdsdisrequiredforvirulenceinburkholderiapseudomallei
AT jenkinschristopherh arabinose5phosphateisomerasekdsdisrequiredforvirulenceinburkholderiapseudomallei
AT scottandrewe arabinose5phosphateisomerasekdsdisrequiredforvirulenceinburkholderiapseudomallei
AT oneillpaula arabinose5phosphateisomerasekdsdisrequiredforvirulenceinburkholderiapseudomallei
AT norvilleisobelh arabinose5phosphateisomerasekdsdisrequiredforvirulenceinburkholderiapseudomallei
AT priorjoannl arabinose5phosphateisomerasekdsdisrequiredforvirulenceinburkholderiapseudomallei
AT irelandphilipm arabinose5phosphateisomerasekdsdisrequiredforvirulenceinburkholderiapseudomallei