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


Journal

BMC microbiology
ISSN: 1471-2180
Titre abrégé: BMC Microbiol
Pays: England
ID NLM: 100966981

Informations de publication

Date de publication:
07 05 2020
Historique:
received: 30 04 2019
accepted: 26 04 2020
entrez: 9 5 2020
pubmed: 10 5 2020
medline: 27 5 2021
Statut: epublish

Résumé

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. 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). 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.

Sections du résumé

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.

Identifiants

pubmed: 32380943
doi: 10.1186/s12866-020-01804-9
pii: 10.1186/s12866-020-01804-9
pmc: PMC7206731
doi:

Substances chimiques

3'-sialyllactose 0
Bacterial Proteins 0
Culture Media 0
Oligosaccharides 0
beta-Galactosidase EC 3.2.1.23
alpha-L-Fucosidase EC 3.2.1.51
beta-N-Acetylhexosaminidases EC 3.2.1.52

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

111

Références

J Dairy Sci. 2003 Apr;86(4):1315-20
pubmed: 12741556
Annu Rev Anim Biosci. 2015;3:419-45
pubmed: 25387230
J Dairy Sci. 2013;96(12):7684-91
pubmed: 24140337
J Dairy Sci. 2015 Nov;98(11):7644-9
pubmed: 26364096
Appl Environ Microbiol. 2014 Oct;80(20):6383-94
pubmed: 25107967
Food Res Int. 2014 Sep 1;63(Pt B):203-209
pubmed: 25284962
Nucleic Acids Res. 2001 May 1;29(9):e45
pubmed: 11328886
PLoS One. 2012;7(5):e36957
pubmed: 22606315
Appl Environ Microbiol. 2015 Nov 20;82(4):980-991
pubmed: 26590291
PLoS One. 2015 Dec 11;10(12):e0144611
pubmed: 26656394
J Dairy Sci. 2008 Oct;91(10):3768-78
pubmed: 18832198
BMC Microbiol. 2013 Oct 29;13:239
pubmed: 24164698
J Dairy Sci. 2012 Nov;95(11):6313-9
pubmed: 22981580
J Food Prot. 2012 Apr;75(4):748-52
pubmed: 22488065
Appl Microbiol Biotechnol. 2014 Jan;98(2):563-77
pubmed: 24287935
World J Gastroenterol. 2014 Oct 7;20(37):13446-52
pubmed: 25309075
Biosci Biotechnol Biochem. 2013;77(3):455-66
pubmed: 23470761
Microb Ecol Health Dis. 2015 Feb 02;26:25877
pubmed: 25651995
Crit Rev Food Sci Nutr. 2002 Jul;42(4):353-75
pubmed: 12180777
Clin Med Insights Pediatr. 2017 Jan 08;10:119-130
pubmed: 28096702
Korean J Food Sci Anim Resour. 2015;35(1):1-9
pubmed: 26761794
Can J Microbiol. 2015 Feb;61(2):93-103
pubmed: 25629960
Appl Environ Microbiol. 2007 Jul;73(13):4259-67
pubmed: 17496132
BMC Pediatr. 2014 Dec 20;14:306
pubmed: 25527244
J Agric Food Chem. 2016 Aug 17;64(32):6364-74
pubmed: 27428379
J Microbiol Methods. 2009 May;77(2):235-42
pubmed: 19248811
FEMS Microbiol Lett. 2016 Jan;363(2):fnv234
pubmed: 26656278
Front Microbiol. 2016 Sep 22;7:1460
pubmed: 27713728
PLoS One. 2013 Jun 21;8(6):e67224
pubmed: 23805302
Syst Appl Microbiol. 2007 Jul;30(5):381-9
pubmed: 17321094
Appl Environ Microbiol. 2009 Feb;75(4):1165-72
pubmed: 19088323
Microbiol Spectr. 2017 Jun;5(3):
pubmed: 28643627
Annu Rev Nutr. 2014;34:143-69
pubmed: 24850388
Annu Rev Food Sci Technol. 2011;2:331-51
pubmed: 22129386
Int Dairy J. 2009 Sep 1;19(9):524-530
pubmed: 20161544
Front Pediatr. 2018 Jul 02;6:190
pubmed: 30013961
Int J Food Microbiol. 2015 Dec 23;215:7-15
pubmed: 26318408
Microbiology. 2013 Apr;159(Pt 4):649-664
pubmed: 23460033
Br J Nutr. 2013 Dec;110(12):2127-37
pubmed: 23710626
J Food Prot. 2013 Oct;76(10):1740-6
pubmed: 24112574
J Food Prot. 2012 Oct;75(10):1796-805
pubmed: 23043828
Foods. 2018 Dec 03;7(12):
pubmed: 30513877
J Dairy Sci. 2009 Jul;92(7):2991-3001
pubmed: 19528576
J Clin Gastroenterol. 2016 Nov/Dec;50 Suppl 2, Proceedings from the 8th Probiotics, Prebiotics & Ne:S131-S132
pubmed: 27741156
Appl Environ Microbiol. 2014 Oct;80(20):6290-302
pubmed: 25085493
J Nutr Sci. 2017 Feb 20;6:e6
pubmed: 28620481
Int J Food Microbiol. 2012 Jun 1;156(3):255-63
pubmed: 22541391
FEMS Microbiol Lett. 2015 Jan;362(1):1-7
pubmed: 25790499
J Food Prot. 2015 Jan;78(1):31-41
pubmed: 25581175
Front Immunol. 2014 Sep 05;5:427
pubmed: 25250028

Auteurs

Pauline Bondue (P)

Department of Food Science, Fundamental and Applied Research for Animal and Health, Faculty of Veterinary Medicine, University of Liège, Liège, Belgium.

Christian Milani (C)

Laboratory of Probiogenomics, Department of Chemistry, Life Sciences and Environmental Sustainability, University of Parma, Parma, Italy.

Emilie Arnould (E)

Department of Food Science, Fundamental and Applied Research for Animal and Health, Faculty of Veterinary Medicine, University of Liège, Liège, Belgium.

Marco Ventura (M)

Laboratory of Probiogenomics, Department of Chemistry, Life Sciences and Environmental Sustainability, University of Parma, Parma, Italy.

Georges Daube (G)

Department of Food Science, Fundamental and Applied Research for Animal and Health, Faculty of Veterinary Medicine, University of Liège, Liège, Belgium.

Gisèle LaPointe (G)

Canadian Research Institute for Food Safety, University of Guelph, Guelph, Canada.

Véronique Delcenserie (V)

Department of Food Science, Fundamental and Applied Research for Animal and Health, Faculty of Veterinary Medicine, University of Liège, Liège, Belgium. Veronique.Delcenserie@ulg.ac.be.

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Classifications MeSH