Cargando…

The Pleiotropic Effects of Carbohydrate-Mediated Growth Rate Modifications in Bifidobacterium longum NCC 2705

Bifidobacteria are saccharolytic bacteria that are able to metabolize a relatively large range of carbohydrates through their unique central carbon metabolism known as the “bifid-shunt”. Carbohydrates have been shown to modulate the growth rate of bifidobacteria, but unlike for other genera (e.g., E...

Descripción completa

Detalles Bibliográficos
Autores principales: Duboux, Stéphane, Pruvost, Solenn, Joyce, Christopher, Bogicevic, Biljana, Muller, Jeroen André, Mercenier, Annick, Kleerebezem, Michiel
Formato: Online Artículo Texto
Lenguaje:English
Publicado: MDPI 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10059941/
https://www.ncbi.nlm.nih.gov/pubmed/36985162
http://dx.doi.org/10.3390/microorganisms11030588
_version_ 1785016995752706048
author Duboux, Stéphane
Pruvost, Solenn
Joyce, Christopher
Bogicevic, Biljana
Muller, Jeroen André
Mercenier, Annick
Kleerebezem, Michiel
author_facet Duboux, Stéphane
Pruvost, Solenn
Joyce, Christopher
Bogicevic, Biljana
Muller, Jeroen André
Mercenier, Annick
Kleerebezem, Michiel
author_sort Duboux, Stéphane
collection PubMed
description Bifidobacteria are saccharolytic bacteria that are able to metabolize a relatively large range of carbohydrates through their unique central carbon metabolism known as the “bifid-shunt”. Carbohydrates have been shown to modulate the growth rate of bifidobacteria, but unlike for other genera (e.g., E. coli or L. lactis), the impact it may have on the overall physiology of the bacteria has not been studied in detail to date. Using glucose and galactose as model substrates in Bifidobacterium longum NCC 2705, we established that the strain displayed fast and slow growth rates on those carbohydrates, respectively. We show that these differential growth conditions are accompanied by global transcriptional changes and adjustments of central carbon fluxes. In addition, when grown on galactose, NCC 2705 cells were significantly smaller, exhibited an expanded capacity to import and metabolized different sugars and displayed an increased acid-stress resistance, a phenotypic signature associated with generalized fitness. We predict that part of the observed adaptation is regulated by the previously described bifidobacterial global transcriptional regulator AraQ, which we propose to reflect a catabolite-repression-like response in B. longum. With this manuscript, we demonstrate that not only growth rate but also various physiological characteristics of B. longum NCC 2705 are responsive to the carbon source used for growth, which is relevant in the context of its lifestyle in the human infant gut where galactose-containing oligosaccharides are prominent.
format Online
Article
Text
id pubmed-10059941
institution National Center for Biotechnology Information
language English
publishDate 2023
publisher MDPI
record_format MEDLINE/PubMed
spelling pubmed-100599412023-03-30 The Pleiotropic Effects of Carbohydrate-Mediated Growth Rate Modifications in Bifidobacterium longum NCC 2705 Duboux, Stéphane Pruvost, Solenn Joyce, Christopher Bogicevic, Biljana Muller, Jeroen André Mercenier, Annick Kleerebezem, Michiel Microorganisms Article Bifidobacteria are saccharolytic bacteria that are able to metabolize a relatively large range of carbohydrates through their unique central carbon metabolism known as the “bifid-shunt”. Carbohydrates have been shown to modulate the growth rate of bifidobacteria, but unlike for other genera (e.g., E. coli or L. lactis), the impact it may have on the overall physiology of the bacteria has not been studied in detail to date. Using glucose and galactose as model substrates in Bifidobacterium longum NCC 2705, we established that the strain displayed fast and slow growth rates on those carbohydrates, respectively. We show that these differential growth conditions are accompanied by global transcriptional changes and adjustments of central carbon fluxes. In addition, when grown on galactose, NCC 2705 cells were significantly smaller, exhibited an expanded capacity to import and metabolized different sugars and displayed an increased acid-stress resistance, a phenotypic signature associated with generalized fitness. We predict that part of the observed adaptation is regulated by the previously described bifidobacterial global transcriptional regulator AraQ, which we propose to reflect a catabolite-repression-like response in B. longum. With this manuscript, we demonstrate that not only growth rate but also various physiological characteristics of B. longum NCC 2705 are responsive to the carbon source used for growth, which is relevant in the context of its lifestyle in the human infant gut where galactose-containing oligosaccharides are prominent. MDPI 2023-02-26 /pmc/articles/PMC10059941/ /pubmed/36985162 http://dx.doi.org/10.3390/microorganisms11030588 Text en © 2023 by the authors. https://creativecommons.org/licenses/by/4.0/Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
spellingShingle Article
Duboux, Stéphane
Pruvost, Solenn
Joyce, Christopher
Bogicevic, Biljana
Muller, Jeroen André
Mercenier, Annick
Kleerebezem, Michiel
The Pleiotropic Effects of Carbohydrate-Mediated Growth Rate Modifications in Bifidobacterium longum NCC 2705
title The Pleiotropic Effects of Carbohydrate-Mediated Growth Rate Modifications in Bifidobacterium longum NCC 2705
title_full The Pleiotropic Effects of Carbohydrate-Mediated Growth Rate Modifications in Bifidobacterium longum NCC 2705
title_fullStr The Pleiotropic Effects of Carbohydrate-Mediated Growth Rate Modifications in Bifidobacterium longum NCC 2705
title_full_unstemmed The Pleiotropic Effects of Carbohydrate-Mediated Growth Rate Modifications in Bifidobacterium longum NCC 2705
title_short The Pleiotropic Effects of Carbohydrate-Mediated Growth Rate Modifications in Bifidobacterium longum NCC 2705
title_sort pleiotropic effects of carbohydrate-mediated growth rate modifications in bifidobacterium longum ncc 2705
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10059941/
https://www.ncbi.nlm.nih.gov/pubmed/36985162
http://dx.doi.org/10.3390/microorganisms11030588
work_keys_str_mv AT dubouxstephane thepleiotropiceffectsofcarbohydratemediatedgrowthratemodificationsinbifidobacteriumlongumncc2705
AT pruvostsolenn thepleiotropiceffectsofcarbohydratemediatedgrowthratemodificationsinbifidobacteriumlongumncc2705
AT joycechristopher thepleiotropiceffectsofcarbohydratemediatedgrowthratemodificationsinbifidobacteriumlongumncc2705
AT bogicevicbiljana thepleiotropiceffectsofcarbohydratemediatedgrowthratemodificationsinbifidobacteriumlongumncc2705
AT mullerjeroenandre thepleiotropiceffectsofcarbohydratemediatedgrowthratemodificationsinbifidobacteriumlongumncc2705
AT mercenierannick thepleiotropiceffectsofcarbohydratemediatedgrowthratemodificationsinbifidobacteriumlongumncc2705
AT kleerebezemmichiel thepleiotropiceffectsofcarbohydratemediatedgrowthratemodificationsinbifidobacteriumlongumncc2705
AT dubouxstephane pleiotropiceffectsofcarbohydratemediatedgrowthratemodificationsinbifidobacteriumlongumncc2705
AT pruvostsolenn pleiotropiceffectsofcarbohydratemediatedgrowthratemodificationsinbifidobacteriumlongumncc2705
AT joycechristopher pleiotropiceffectsofcarbohydratemediatedgrowthratemodificationsinbifidobacteriumlongumncc2705
AT bogicevicbiljana pleiotropiceffectsofcarbohydratemediatedgrowthratemodificationsinbifidobacteriumlongumncc2705
AT mullerjeroenandre pleiotropiceffectsofcarbohydratemediatedgrowthratemodificationsinbifidobacteriumlongumncc2705
AT mercenierannick pleiotropiceffectsofcarbohydratemediatedgrowthratemodificationsinbifidobacteriumlongumncc2705
AT kleerebezemmichiel pleiotropiceffectsofcarbohydratemediatedgrowthratemodificationsinbifidobacteriumlongumncc2705