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Arabinogalactan Utilization by Bifidobacterium longum subsp. longum NCC 2705 and Bacteroides caccae ATCC 43185 in Monoculture and Coculture

Arabinogalactan (AG) has been studied as a potential prebiotic in view of stimulating bifidobacteria presence in the gut microbiota. However, bifidobacteria prefer fermentation of oligosaccharides to that of polysaccharides. The contribution of other gut bacteria may allow better growth of bifidobac...

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Autores principales: Wang, Yan, LaPointe, Gisèle
Formato: Online Artículo Texto
Lenguaje:English
Publicado: MDPI 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7693162/
https://www.ncbi.nlm.nih.gov/pubmed/33142707
http://dx.doi.org/10.3390/microorganisms8111703
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author Wang, Yan
LaPointe, Gisèle
author_facet Wang, Yan
LaPointe, Gisèle
author_sort Wang, Yan
collection PubMed
description Arabinogalactan (AG) has been studied as a potential prebiotic in view of stimulating bifidobacteria presence in the gut microbiota. However, bifidobacteria prefer fermentation of oligosaccharides to that of polysaccharides. The contribution of other gut bacteria may allow better growth of bifidobacteria on AG. β-galactanases and β-galactosidases are the main enzymes for the degradation of AG. Additional enzymes such as α-L-arabinofuranosidase and β-L-arabinopyranosidase are required to remove the arabinose side chains. All of these predicted functions are encoded by the genomes of both Bifidobacterium longum subsp. longum NCC 2705 and Bacteroides caccae ATCC 43185. However, neither strain was able to grow significantly on AG, with 25% (B. longum subsp. longum NCC 2705) and 39% (Bac. caccae ATCC 43185) of AG degraded after 48-h fermentation, respectively. In this study, the β-galactanase, β-galactosidase, α-L-arabinofuranosidase, and β-L-arabinopyranosidase from both strains were investigated. The extracellular β-galactosidases of both B. longum subsp. longum NCC 2705 and Bac. caccae ATCC 43185 were able to cleave the β-1,3; 1,4 and 1,6 linkages. However, the β-galactosidase activity of B. longum subsp. longum NCC 2705 was weaker for the β-1,4 linkage, compared with the β-1,3 and 1,6 linkages. The arabinose side chains of AG inhibited the cleavage of β-1,3 and 1,6 linkages by the endo-β-galactanase from both strains, and partially inhibited the cleavage of β-1,4 linkages by the endo-β-1,4 galactanase from Bac. caccae ATCC 43185. The α-L-arabinofuranosidase and β-L-arabinopyranosidase from both strains were unable to cleave arabinose from AG under the conditions used. These results show limited breakdown of AG by these two strains in monoculture. When cocultured with Bac. caccae ATCC 43185, B. longum subsp. longum NCC 2705 grew significantly better than in monoculture on AG after 6 h of fermentation (p < 0.05). The coculture showed 48% AG degradation after 48 h of fermentation, along with reduced pH. Furthermore, compared to monoculture of Bac. caccae ATCC 43185, the concentration of succinate significantly increased from 0.01 ± 0.01 to 4.41 ± 0.61 mM, whereas propionate significantly decreased from 13.07 ± 0.37 to 9.75 ± 2.01 mM in the coculture (p < 0.05). These results suggest that the growth and metabolic activities of Bac. caccae ATCC 43185 were restrained in the coculture, as the pH decreased due to the metabolism of B. longum subsp. longum NCC 2705.
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spelling pubmed-76931622020-11-28 Arabinogalactan Utilization by Bifidobacterium longum subsp. longum NCC 2705 and Bacteroides caccae ATCC 43185 in Monoculture and Coculture Wang, Yan LaPointe, Gisèle Microorganisms Article Arabinogalactan (AG) has been studied as a potential prebiotic in view of stimulating bifidobacteria presence in the gut microbiota. However, bifidobacteria prefer fermentation of oligosaccharides to that of polysaccharides. The contribution of other gut bacteria may allow better growth of bifidobacteria on AG. β-galactanases and β-galactosidases are the main enzymes for the degradation of AG. Additional enzymes such as α-L-arabinofuranosidase and β-L-arabinopyranosidase are required to remove the arabinose side chains. All of these predicted functions are encoded by the genomes of both Bifidobacterium longum subsp. longum NCC 2705 and Bacteroides caccae ATCC 43185. However, neither strain was able to grow significantly on AG, with 25% (B. longum subsp. longum NCC 2705) and 39% (Bac. caccae ATCC 43185) of AG degraded after 48-h fermentation, respectively. In this study, the β-galactanase, β-galactosidase, α-L-arabinofuranosidase, and β-L-arabinopyranosidase from both strains were investigated. The extracellular β-galactosidases of both B. longum subsp. longum NCC 2705 and Bac. caccae ATCC 43185 were able to cleave the β-1,3; 1,4 and 1,6 linkages. However, the β-galactosidase activity of B. longum subsp. longum NCC 2705 was weaker for the β-1,4 linkage, compared with the β-1,3 and 1,6 linkages. The arabinose side chains of AG inhibited the cleavage of β-1,3 and 1,6 linkages by the endo-β-galactanase from both strains, and partially inhibited the cleavage of β-1,4 linkages by the endo-β-1,4 galactanase from Bac. caccae ATCC 43185. The α-L-arabinofuranosidase and β-L-arabinopyranosidase from both strains were unable to cleave arabinose from AG under the conditions used. These results show limited breakdown of AG by these two strains in monoculture. When cocultured with Bac. caccae ATCC 43185, B. longum subsp. longum NCC 2705 grew significantly better than in monoculture on AG after 6 h of fermentation (p < 0.05). The coculture showed 48% AG degradation after 48 h of fermentation, along with reduced pH. Furthermore, compared to monoculture of Bac. caccae ATCC 43185, the concentration of succinate significantly increased from 0.01 ± 0.01 to 4.41 ± 0.61 mM, whereas propionate significantly decreased from 13.07 ± 0.37 to 9.75 ± 2.01 mM in the coculture (p < 0.05). These results suggest that the growth and metabolic activities of Bac. caccae ATCC 43185 were restrained in the coculture, as the pH decreased due to the metabolism of B. longum subsp. longum NCC 2705. MDPI 2020-10-31 /pmc/articles/PMC7693162/ /pubmed/33142707 http://dx.doi.org/10.3390/microorganisms8111703 Text en © 2020 by the authors. 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 (http://creativecommons.org/licenses/by/4.0/).
spellingShingle Article
Wang, Yan
LaPointe, Gisèle
Arabinogalactan Utilization by Bifidobacterium longum subsp. longum NCC 2705 and Bacteroides caccae ATCC 43185 in Monoculture and Coculture
title Arabinogalactan Utilization by Bifidobacterium longum subsp. longum NCC 2705 and Bacteroides caccae ATCC 43185 in Monoculture and Coculture
title_full Arabinogalactan Utilization by Bifidobacterium longum subsp. longum NCC 2705 and Bacteroides caccae ATCC 43185 in Monoculture and Coculture
title_fullStr Arabinogalactan Utilization by Bifidobacterium longum subsp. longum NCC 2705 and Bacteroides caccae ATCC 43185 in Monoculture and Coculture
title_full_unstemmed Arabinogalactan Utilization by Bifidobacterium longum subsp. longum NCC 2705 and Bacteroides caccae ATCC 43185 in Monoculture and Coculture
title_short Arabinogalactan Utilization by Bifidobacterium longum subsp. longum NCC 2705 and Bacteroides caccae ATCC 43185 in Monoculture and Coculture
title_sort arabinogalactan utilization by bifidobacterium longum subsp. longum ncc 2705 and bacteroides caccae atcc 43185 in monoculture and coculture
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7693162/
https://www.ncbi.nlm.nih.gov/pubmed/33142707
http://dx.doi.org/10.3390/microorganisms8111703
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