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Integrating proteomic data with metabolic modeling provides insight into key pathways of Bordetella pertussis biofilms

Pertussis, commonly known as whooping cough is a severe respiratory disease caused by the bacterium, Bordetella pertussis. Despite widespread vaccination, pertussis resurgence has been observed globally. The development of the current acellular vaccine (ACV) has been based on planktonic studies. How...

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Autores principales: Suyama, Hiroki, Luu, Laurence Don Wai, Zhong, Ling, Raftery, Mark J., Lan, Ruiting
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10435875/
https://www.ncbi.nlm.nih.gov/pubmed/37601354
http://dx.doi.org/10.3389/fmicb.2023.1169870
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author Suyama, Hiroki
Luu, Laurence Don Wai
Zhong, Ling
Raftery, Mark J.
Lan, Ruiting
author_facet Suyama, Hiroki
Luu, Laurence Don Wai
Zhong, Ling
Raftery, Mark J.
Lan, Ruiting
author_sort Suyama, Hiroki
collection PubMed
description Pertussis, commonly known as whooping cough is a severe respiratory disease caused by the bacterium, Bordetella pertussis. Despite widespread vaccination, pertussis resurgence has been observed globally. The development of the current acellular vaccine (ACV) has been based on planktonic studies. However, recent studies have shown that B. pertussis readily forms biofilms. A better understanding of B. pertussis biofilms is important for developing novel vaccines that can target all aspects of B. pertussis infection. This study compared the proteomic expression of biofilm and planktonic B. pertussis cells to identify key changes between the conditions. Major differences were identified in virulence factors including an upregulation of toxins (adenylate cyclase toxin and dermonecrotic toxin) and downregulation of pertactin and type III secretion system proteins in biofilm cells. To further dissect metabolic pathways that are altered during the biofilm lifestyle, the proteomic data was then incorporated into a genome scale metabolic model using the Integrative Metabolic Analysis Tool (iMAT). The generated models predicted that planktonic cells utilised the glyoxylate shunt while biofilm cells completed the full tricarboxylic acid cycle. Differences in processing aspartate, arginine and alanine were identified as well as unique export of valine out of biofilm cells which may have a role in inter-bacterial communication and regulation. Finally, increased polyhydroxybutyrate accumulation and superoxide dismutase activity in biofilm cells may contribute to increased persistence during infection. Taken together, this study modeled major proteomic and metabolic changes that occur in biofilm cells which helps lay the groundwork for further understanding B. pertussis pathogenesis.
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spelling pubmed-104358752023-08-19 Integrating proteomic data with metabolic modeling provides insight into key pathways of Bordetella pertussis biofilms Suyama, Hiroki Luu, Laurence Don Wai Zhong, Ling Raftery, Mark J. Lan, Ruiting Front Microbiol Microbiology Pertussis, commonly known as whooping cough is a severe respiratory disease caused by the bacterium, Bordetella pertussis. Despite widespread vaccination, pertussis resurgence has been observed globally. The development of the current acellular vaccine (ACV) has been based on planktonic studies. However, recent studies have shown that B. pertussis readily forms biofilms. A better understanding of B. pertussis biofilms is important for developing novel vaccines that can target all aspects of B. pertussis infection. This study compared the proteomic expression of biofilm and planktonic B. pertussis cells to identify key changes between the conditions. Major differences were identified in virulence factors including an upregulation of toxins (adenylate cyclase toxin and dermonecrotic toxin) and downregulation of pertactin and type III secretion system proteins in biofilm cells. To further dissect metabolic pathways that are altered during the biofilm lifestyle, the proteomic data was then incorporated into a genome scale metabolic model using the Integrative Metabolic Analysis Tool (iMAT). The generated models predicted that planktonic cells utilised the glyoxylate shunt while biofilm cells completed the full tricarboxylic acid cycle. Differences in processing aspartate, arginine and alanine were identified as well as unique export of valine out of biofilm cells which may have a role in inter-bacterial communication and regulation. Finally, increased polyhydroxybutyrate accumulation and superoxide dismutase activity in biofilm cells may contribute to increased persistence during infection. Taken together, this study modeled major proteomic and metabolic changes that occur in biofilm cells which helps lay the groundwork for further understanding B. pertussis pathogenesis. Frontiers Media S.A. 2023-08-03 /pmc/articles/PMC10435875/ /pubmed/37601354 http://dx.doi.org/10.3389/fmicb.2023.1169870 Text en Copyright © 2023 Suyama, Luu, Zhong, Raftery and Lan. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Microbiology
Suyama, Hiroki
Luu, Laurence Don Wai
Zhong, Ling
Raftery, Mark J.
Lan, Ruiting
Integrating proteomic data with metabolic modeling provides insight into key pathways of Bordetella pertussis biofilms
title Integrating proteomic data with metabolic modeling provides insight into key pathways of Bordetella pertussis biofilms
title_full Integrating proteomic data with metabolic modeling provides insight into key pathways of Bordetella pertussis biofilms
title_fullStr Integrating proteomic data with metabolic modeling provides insight into key pathways of Bordetella pertussis biofilms
title_full_unstemmed Integrating proteomic data with metabolic modeling provides insight into key pathways of Bordetella pertussis biofilms
title_short Integrating proteomic data with metabolic modeling provides insight into key pathways of Bordetella pertussis biofilms
title_sort integrating proteomic data with metabolic modeling provides insight into key pathways of bordetella pertussis biofilms
topic Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10435875/
https://www.ncbi.nlm.nih.gov/pubmed/37601354
http://dx.doi.org/10.3389/fmicb.2023.1169870
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