Cross-feeding interactions between human gut commensals belonging to the Bacteroides and Bifidobacterium genera when grown on dietary glycans

Pedro Fernandez-Julia , Daniel M. Commane , Douwe van Sinderen , Jose Munoz-Munoz

Microbiome Research Reports ›› 2022, Vol. 1 ›› Issue (2) : 12

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Microbiome Research Reports ›› 2022, Vol. 1 ›› Issue (2) :12 DOI: 10.20517/mrr.2021.05
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Cross-feeding interactions between human gut commensals belonging to the Bacteroides and Bifidobacterium genera when grown on dietary glycans

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Abstract

Elements of the human gut microbiota metabolise many host- and diet-derived, non-digestible carbohydrates (NDCs). Intestinal fermentation of NDCs salvages energy and resources for the host and generates beneficial metabolites, such as short chain fatty acids, which contribute to host health. The development of functional NDCs that support the growth and/or metabolic activity of specific beneficial gut bacteria, is desirable, but dependent on an in-depth understanding of the pathways of carbohydrate fermentation. The purpose of this review is to provide an appraisal of what is known about the roles of, and interactions between, Bacteroides and Bifidobacterium as key members involved in NDC utilisation. Bacteroides is considered an important primary degrader of complex NDCs, thereby generating oligosaccharides, which in turn can be fermented by secondary degraders. In this review, we will therefore focus on Bacteroides as an NDC-degrading specialist and Bifidobacterium as an important and purported probiotic representative of secondary degraders. We will describe cross-feeding interactions between members of these two genera. We note that there are limited studies exploring the interactions between Bacteroides and Bifidobacterium, specifically concerning β-glucan and arabinoxylan metabolism. This review therefore summarises the roles of these organisms in the breakdown of dietary fibre and the molecular mechanisms and interactions involved. Finally, it also highlights the need for further research into the phenomenon of cross-feeding between these organisms for an improved understanding of these cross-feeding mechanisms to guide the rational development of prebiotics to support host health or to prevent or combat disease associated with microbial dysbiosis.

Keywords

Cross-feeding / plant fibre / Bacteroides / Bifidobacterium / gut microbiota / prebiotic

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Pedro Fernandez-Julia, Daniel M. Commane, Douwe van Sinderen, Jose Munoz-Munoz. Cross-feeding interactions between human gut commensals belonging to the Bacteroides and Bifidobacterium genera when grown on dietary glycans. Microbiome Research Reports, 2022, 1(2): 12 DOI:10.20517/mrr.2021.05

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References

[1]

Thursby E.Introduction to the human gut microbiota.Biochem J2017;474:1823-36 PMCID:PMC5433529

[2]

Belizário JE.Human microbiomes and their roles in dysbiosis, common diseases, and novel therapeutic approaches.Front Microbiol2015;6:1050 PMCID:PMC4594012

[3]

Mar JS,Lin DL.Disease severity and immune activity relate to distinct interkingdom gut microbiome states in ethnically distinct ulcerative colitis patients.mBio2016;7:e01072-16 PMCID:PMC4992973

[4]

Stewart CJ,O’Brien JL.Temporal development of the gut microbiome in early childhood from the TEDDY study.Nature2018;562:583-8 PMCID:PMC6415775

[5]

Hamaker BR.A perspective on the complexity of dietary fiber structures and their potential effect on the gut microbiota.J Mol Biol2014;426:3838-50

[6]

Grondin JM,Déjean G,Brumer H.Polysaccharide utilization loci: fueling microbial communities.J Bacteriol2017;199:e00860-16 PMCID:PMC5512228

[7]

McNeil NI.The contribution of the large intestine to energy supplies in man.Am J Clin Nutr1984;39:338-42

[8]

Le Poul E,Struyf S.Functional characterization of human receptors for short chain fatty acids and their role in polymorphonuclear cell activation.J Biol Chem2003;278:25481-9

[9]

Parada Venegas D,Landskron G.Short chain fatty acids (SCFAs)-mediated gut epithelial and immune regulation and its relevance for inflammatory bowel diseases.Front Immunol2019;10:277 PMCID:PMC6421268

[10]

Besten G, van Eunen K, Groen AK, Venema K, Reijngoud DJ, Bakker BM. The role of short-chain fatty acids in the interplay between diet, gut microbiota, and host energy metabolism.J Lipid Res2013;54:2325-40 PMCID:PMC3735932

[11]

Ang Z.GPR41 and GPR43 in obesity and inflammation - protective or causative?.Front Immunol2016;7:28 PMCID:PMC4734206

[12]

Lapébie P,Drula E,Henrissat B.Bacteroidetes use thousands of enzyme combinations to break down glycans.Nat Commun2019;10:2043 PMCID:PMC6499787

[13]

Larsbrink L,Bacteroidetes bacteria in the soil: Glycan acquisition.Adv Appl Microbiol 2020;110:63-98.

[14]

Koropatkin NM,Martens EC.How glycan metabolism shapes the human gut microbiota.Nat Rev Microbiol2012;10:323-35 PMCID:PMC4005082

[15]

O Sheridan P,Lawley TD.Polysaccharide utilization loci and nutritional specialization in a dominant group of butyrate-producing human colonic Firmicutes.Microb Genom2016;2:e000043 PMCID:PMC5320581

[16]

Van der Meulen R,Verbrugghe K.Kinetic analysis of bifidobacterial metabolism reveals a minor role for succinic acid in the regeneration of NAD+ through its growth-associated production.Appl Environ Microbiol2006;72:5204-10 PMCID:PMC1538715

[17]

Turroni F,Duranti S,van Sinderen D.Glycan utilization and cross-feeding activities by Bifidobacteria.Trends Microbiol2018;26:339-50

[18]

Singh RP.Glycan utilisation system in Bacteroides and Bifidobacteria and their roles in gut stability and health.Appl Microbiol Biotechnol2019;103:7287-315

[19]

Egan M,Ventura M.Metabolism of sialic acid by Bifidobacterium breve UCC2003.Appl Environ Microbiol2014;80:4414-26 PMCID:PMC4068672

[20]

Turroni F,Milani C.Glycan cross-feeding activities between bifidobacteria under in vitro conditions.Front Microbiol2015;6:1030 PMCID:PMC4585166

[21]

Cheng CC,Lin X.Ecological importance of cross-feeding of the intermediate metabolite 1,2-propanediol between bacterial gut symbionts.Appl Environ Microbiol2020;86:e00190-20 PMCID:PMC7237793

[22]

Smith NW,Altermann E,Mcnabb WC.The classification and evolution of bacterial cross-feeding.Front Ecol Evol2019;7:153

[23]

Morris BE,Huber H.Microbial syntrophy: interaction for the common good.FEMS Microbiol Rev2013;37:384-406

[24]

Schwalm ND 3rd.Navigating the gut buffet: control of polysaccharide utilization in Bacteroides spp.Trends Microbiol2017;25:1005-15

[25]

Rakoff-Nahoum S,Comstock LE.An ecological network of polysaccharide utilization among human intestinal symbionts.Curr Biol2014;24:40-9 PMCID:PMC3924574

[26]

Salyers AA,O’Brien M.Utilization of xylan by two species of human colonic Bacteroides.Appl Environ Microbiol1981;41:1065-8 PMCID:PMC243861

[27]

Rakoff-Nahoum S,Comstock LE.The evolution of cooperation within the gut microbiota.Nature2016;533:255-9 PMCID:PMC4978124

[28]

Turroni F,Duranti S.Deciphering bifidobacterial-mediated metabolic interactions and their impact on gut microbiota by a multi-omics approach.ISME J2016;10:1656-68 PMCID:PMC4918443

[29]

Milani C,Duranti S.Bifidobacteria exhibit social behavior through carbohydrate resource sharing in the gut.Sci Rep2015;5:15782 PMCID:PMC4623478

[30]

Egan M,Kilcoyne M.Cross-feeding by Bifidobacterium breve UCC2003 during co-cultivation with Bifidobacterium bifidum PRL2010 in a mucin-based medium.BMC Microbiol2014;14:282 PMCID:PMC4252021

[31]

Turroni F,Foroni E.Genome analysis of Bifidobacterium bifidum PRL2010 reveals metabolic pathways for host-derived glycan foraging.Proc Natl Acad Sci U S A2010;107:19514-9 PMCID:PMC2984195

[32]

Hehemann JH,Barbeyron T,Czjzek M.Transfer of carbohydrate-active enzymes from marine bacteria to Japanese gut microbiota.Nature2010;464:908-12

[33]

Fischbach MA.Eating for two: how metabolism establishes interspecies interactions in the gut.Cell Host Microbe2011;10:336-47 PMCID:PMC3225337

[34]

Rios-Covian D,Hernandez-Barranco AM.Interactions between Bifidobacterium and Bacteroides species in cofermentations are affected by carbon sources, including exopolysaccharides produced by bifidobacteria.Appl Environ Microbiol2013;79:7518-24 PMCID:PMC3837738

[35]

Rogowski A,Mortimer JC.Glycan complexity dictates microbial resource allocation in the large intestine.Nat Commun2015;6:7481 PMCID:PMC4491172

[36]

Zeybek N,Buyukkileci AO.Utilization of xylan-type polysaccharides in co-culture fermentations of Bifidobacterium and Bacteroides species.Carbohydr Polym2020;236:116076

[37]

Falony G,Verschaeren A,Maes D.In vitro kinetic analysis of fermentation of prebiotic inulin-type fructans by Bifidobacterium species reveals four different phenotypes.Appl Environ Microbiol2009;75:454-61 PMCID:PMC2620708

[38]

Munoz J,Bottacini F.Biochemical analysis of cross-feeding behaviour between two common gut commensals when cultivated on plant-derived arabinogalactan.Microb Biotechnol2020;13:1733-47 PMCID:PMC7533333

[39]

Liu Y,Galland B.Substrate use prioritization by a coculture of five species of gut bacteria fed mixtures of arabinoxylan, xyloglucan, β-glucan, and pectin.Appl Environ Microbiol2020;86:e01905-19 PMCID:PMC6952225

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