Bifidobacterium mongoliense genome seems particularly adapted to milk oligosaccharide digestion leading to production of antivirulent metabolites

Abstract Background Human milk oligosaccharides (HMO) could promote the growth of bifidobacteria, improving young children’s health. In addition, fermentation of carbohydrates by bifidobacteria can result in the production of metabolites presenting an antivirulent activity against intestinal pathoge...

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Main Authors: Pauline Bondue, Christian Milani, Emilie Arnould, Marco Ventura, Georges Daube, Gisèle LaPointe, Véronique Delcenserie
Format: Article
Language:English
Published: BMC 2020-05-01
Series:BMC Microbiology
Subjects:
Online Access:http://link.springer.com/article/10.1186/s12866-020-01804-9
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spelling doaj-60976b4f194548a38e611a261d6517772020-11-25T02:12:11ZengBMCBMC Microbiology1471-21802020-05-0120111210.1186/s12866-020-01804-9Bifidobacterium mongoliense genome seems particularly adapted to milk oligosaccharide digestion leading to production of antivirulent metabolitesPauline Bondue0Christian Milani1Emilie Arnould2Marco Ventura3Georges Daube4Gisèle LaPointe5Véronique Delcenserie6Department of Food Science, Fundamental and Applied Research for Animal and Health, Faculty of Veterinary Medicine, University of LiègeLaboratory of Probiogenomics, Department of Chemistry, Life Sciences and Environmental Sustainability, University of ParmaDepartment of Food Science, Fundamental and Applied Research for Animal and Health, Faculty of Veterinary Medicine, University of LiègeLaboratory of Probiogenomics, Department of Chemistry, Life Sciences and Environmental Sustainability, University of ParmaDepartment of Food Science, Fundamental and Applied Research for Animal and Health, Faculty of Veterinary Medicine, University of LiègeCanadian Research Institute for Food Safety, University of GuelphDepartment of Food Science, Fundamental and Applied Research for Animal and Health, Faculty of Veterinary Medicine, University of LiègeAbstract Background Human milk oligosaccharides (HMO) could promote the growth of bifidobacteria, improving young children’s health. In addition, fermentation of carbohydrates by bifidobacteria can result in the production of metabolites presenting an antivirulent activity against intestinal pathogens. Bovine milk oligosaccharides (BMO), structurally similar to HMO, are found at high concentration in cow whey. This is particularly observed for 3′-sialyllactose (3′SL). This study focused on enzymes and transport systems involved in HMO/BMO metabolism contained in B. crudilactis and B. mongoliense genomes, two species from bovine milk origin. The ability of B. mongoliense to grow in media supplemented with whey or 3′SL was assessed. Next, the effects of cell-free spent media (CFSM) were tested against the virulence expression of Escherichia coli O157:H7 and Salmonella enterica serovar Typhimurium. Results Due to the presence of genes encoding β-galactosidases, β-hexosaminidases, α-sialidases and α-fucosidases, B. mongoliense presents a genome more sophisticated and more adapted to the digestion of BMO/HMO than B. crudilactis (which contains only β-galactosidases). In addition, HMO/BMO digestion involves genes encoding oligosaccharide transport systems found in B. mongoliense but not in B. crudilactis. B. mongoliense seemed able to grow on media supplemented with whey or 3′SL as main source of carbon (8.3 ± 1.0 and 6.7 ± 0.3 log cfu/mL, respectively). CFSM obtained from whey resulted in a significant under-expression of ler, fliC, luxS, stx1 and qseA genes (− 2.2, − 5.3, − 2.4, − 2.5 and − 4.8, respectively; P < 0.05) of E. coli O157:H7. CFSM from 3′SL resulted in a significant up-regulation of luxS (2.0; P < 0.05) gene and a down-regulation of fliC (− 5.0; P < 0.05) gene. CFSM obtained from whey resulted in significant up-regulations of sopD and hil genes (2.9 and 3.5, respectively; P < 0.05) of S. Typhimurium, while CFSM obtained from 3′SL fermentation down-regulated hil and sopD genes (− 2.7 and − 4.2, respectively; P < 0.05). Conclusion From enzymes and transporters highlighted in the genome of B. mongoliense and its potential ability to metabolise 3′SL and whey, B. mongoliense seems well able to digest HMO/BMO. The exact nature of the metabolites contained in CFSM has to be identified still. These results suggest that BMO associated with B. mongoliense could be an interesting synbiotic formulation to maintain or restore intestinal health of young children.http://link.springer.com/article/10.1186/s12866-020-01804-9Bifidobacterium mongolienseBifidobacterium crudilactisWheyBovine milk oligosaccharide3′-sialyllactoseAntivirulent effect
collection DOAJ
language English
format Article
sources DOAJ
author Pauline Bondue
Christian Milani
Emilie Arnould
Marco Ventura
Georges Daube
Gisèle LaPointe
Véronique Delcenserie
spellingShingle Pauline Bondue
Christian Milani
Emilie Arnould
Marco Ventura
Georges Daube
Gisèle LaPointe
Véronique Delcenserie
Bifidobacterium mongoliense genome seems particularly adapted to milk oligosaccharide digestion leading to production of antivirulent metabolites
BMC Microbiology
Bifidobacterium mongoliense
Bifidobacterium crudilactis
Whey
Bovine milk oligosaccharide
3′-sialyllactose
Antivirulent effect
author_facet Pauline Bondue
Christian Milani
Emilie Arnould
Marco Ventura
Georges Daube
Gisèle LaPointe
Véronique Delcenserie
author_sort Pauline Bondue
title Bifidobacterium mongoliense genome seems particularly adapted to milk oligosaccharide digestion leading to production of antivirulent metabolites
title_short Bifidobacterium mongoliense genome seems particularly adapted to milk oligosaccharide digestion leading to production of antivirulent metabolites
title_full Bifidobacterium mongoliense genome seems particularly adapted to milk oligosaccharide digestion leading to production of antivirulent metabolites
title_fullStr Bifidobacterium mongoliense genome seems particularly adapted to milk oligosaccharide digestion leading to production of antivirulent metabolites
title_full_unstemmed Bifidobacterium mongoliense genome seems particularly adapted to milk oligosaccharide digestion leading to production of antivirulent metabolites
title_sort bifidobacterium mongoliense genome seems particularly adapted to milk oligosaccharide digestion leading to production of antivirulent metabolites
publisher BMC
series BMC Microbiology
issn 1471-2180
publishDate 2020-05-01
description Abstract Background Human milk oligosaccharides (HMO) could promote the growth of bifidobacteria, improving young children’s health. In addition, fermentation of carbohydrates by bifidobacteria can result in the production of metabolites presenting an antivirulent activity against intestinal pathogens. Bovine milk oligosaccharides (BMO), structurally similar to HMO, are found at high concentration in cow whey. This is particularly observed for 3′-sialyllactose (3′SL). This study focused on enzymes and transport systems involved in HMO/BMO metabolism contained in B. crudilactis and B. mongoliense genomes, two species from bovine milk origin. The ability of B. mongoliense to grow in media supplemented with whey or 3′SL was assessed. Next, the effects of cell-free spent media (CFSM) were tested against the virulence expression of Escherichia coli O157:H7 and Salmonella enterica serovar Typhimurium. Results Due to the presence of genes encoding β-galactosidases, β-hexosaminidases, α-sialidases and α-fucosidases, B. mongoliense presents a genome more sophisticated and more adapted to the digestion of BMO/HMO than B. crudilactis (which contains only β-galactosidases). In addition, HMO/BMO digestion involves genes encoding oligosaccharide transport systems found in B. mongoliense but not in B. crudilactis. B. mongoliense seemed able to grow on media supplemented with whey or 3′SL as main source of carbon (8.3 ± 1.0 and 6.7 ± 0.3 log cfu/mL, respectively). CFSM obtained from whey resulted in a significant under-expression of ler, fliC, luxS, stx1 and qseA genes (− 2.2, − 5.3, − 2.4, − 2.5 and − 4.8, respectively; P < 0.05) of E. coli O157:H7. CFSM from 3′SL resulted in a significant up-regulation of luxS (2.0; P < 0.05) gene and a down-regulation of fliC (− 5.0; P < 0.05) gene. CFSM obtained from whey resulted in significant up-regulations of sopD and hil genes (2.9 and 3.5, respectively; P < 0.05) of S. Typhimurium, while CFSM obtained from 3′SL fermentation down-regulated hil and sopD genes (− 2.7 and − 4.2, respectively; P < 0.05). Conclusion From enzymes and transporters highlighted in the genome of B. mongoliense and its potential ability to metabolise 3′SL and whey, B. mongoliense seems well able to digest HMO/BMO. The exact nature of the metabolites contained in CFSM has to be identified still. These results suggest that BMO associated with B. mongoliense could be an interesting synbiotic formulation to maintain or restore intestinal health of young children.
topic Bifidobacterium mongoliense
Bifidobacterium crudilactis
Whey
Bovine milk oligosaccharide
3′-sialyllactose
Antivirulent effect
url http://link.springer.com/article/10.1186/s12866-020-01804-9
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