Journal Home > Volume 11 , Issue 5
Food Science and Human Wellness 2022, 11(5): 1101-1110 https://doi.org/10.1016/j.fshw.2022.04.002
Review Article | Open Access | Issue | Published: 02 June 2022

Bacteroides utilization for dietary polysaccharides and their beneficial effects on gut health

Show Author's Information Jiaobo Chenga,  Jielun Hua,  Fang Gengb,  Shaoping Niea( )
State Key Laboratory of Food Science and Technology, China-Canada Joint Lab of Food Science and Technology (Nanchang), Nanchang University, Nanchang 330047, China
Key Laboratory of Coarse Cereal Processing (Ministry of Agriculture and Rural Affairs), School of Food and Biological Engineering, Chengdu University, Chengdu 610106, China

Peer review under responsibility of KeAi Communications Co., Ltd.

Keywords:
Degradation, Short-chain fatty acids, Polysaccharides, Bacteroides, Gut health
Cite this article:
Cheng J, Hu J, Geng F, et al. Bacteroides utilization for dietary polysaccharides and their beneficial effects on gut health. Food Science and Human Wellness, 2022, 11(5): 1101-1110. https://doi.org/10.1016/j.fshw.2022.04.002
Download citation
EndNote(RIS)
BibTeX

453

Views

40

Downloads

Citations

63

Crossref

54

WoS

54

Scopus

0

CSCD

Abstract Full text About this article

Polysaccharide was a class of macromolecular substance with various bioactive functions. Gut symbiotic microorganisms could utilize the polysaccharides from various sources, thus have important impact on human health. Bacteroides represented one of the dominant colonizers in the human gut. The utilization of polysaccharide by Bacteroides was important for supporting the function and stability of gut microbiota. After the degradation of polysaccharides by Bacteroides, gut microbes could ferment the monosaccharides and oligosaccharides degraded from polysaccharides into some metabolites, such as short-chain fatty acids (SCFAs), amino acids, etc. Among the metabolites, the SCFAs could have beneficial effects on gut health. This review summarized the niches of Bacteroides among gut microbiota, and also described the gene clusters and membrane proteins involved in the utilization processes of polysaccharide by gut Bacteroides. SCFAs could act as energy substrates for intestinal epithelial cells, inhibit histone deacetylases and activate G protein-coupled receptors. In addition, the future perspectives in investigating new degradation pathways for polysaccharide, and using polysaccharides or their metabolites as therapeutic approaches for diseases mediated by the gut dysbiosis were also provided.


menu
Abstract
Full text
Outline
About this article

Bacteroides utilization for dietary polysaccharides and their beneficial effects on gut health

Show Author's information Jiaobo Chenga, Jielun Hua, Fang Gengb, Shaoping Niea( )
State Key Laboratory of Food Science and Technology, China-Canada Joint Lab of Food Science and Technology (Nanchang), Nanchang University, Nanchang 330047, China
Key Laboratory of Coarse Cereal Processing (Ministry of Agriculture and Rural Affairs), School of Food and Biological Engineering, Chengdu University, Chengdu 610106, China

Peer review under responsibility of KeAi Communications Co., Ltd.

Abstract

Polysaccharide was a class of macromolecular substance with various bioactive functions. Gut symbiotic microorganisms could utilize the polysaccharides from various sources, thus have important impact on human health. Bacteroides represented one of the dominant colonizers in the human gut. The utilization of polysaccharide by Bacteroides was important for supporting the function and stability of gut microbiota. After the degradation of polysaccharides by Bacteroides, gut microbes could ferment the monosaccharides and oligosaccharides degraded from polysaccharides into some metabolites, such as short-chain fatty acids (SCFAs), amino acids, etc. Among the metabolites, the SCFAs could have beneficial effects on gut health. This review summarized the niches of Bacteroides among gut microbiota, and also described the gene clusters and membrane proteins involved in the utilization processes of polysaccharide by gut Bacteroides. SCFAs could act as energy substrates for intestinal epithelial cells, inhibit histone deacetylases and activate G protein-coupled receptors. In addition, the future perspectives in investigating new degradation pathways for polysaccharide, and using polysaccharides or their metabolites as therapeutic approaches for diseases mediated by the gut dysbiosis were also provided.

Keywords: Degradation, Short-chain fatty acids, Polysaccharides, Bacteroides, Gut health

References(113)

[1]

A.B. Hall, A.C. Tolonen, R.J. Xavier, Human genetic variation and the gut microbiome in disease, Nat. Rev. Genet. 18 (2017) 690-699. https://doi.org/10.1038/nrg.2017.63
DOI Google Scholar
[2]

Y. Zou, W. Xue, G. Luo, et al., 1,520 reference genomes from cultivated human gut bacteria enable functional microbiome analyses, Nat. Biotechnol. 37 (2019) 179-185. https://doi.org/10.1038/s41587-018-0008-8
DOI Google Scholar
[3]

K.J. Portune, A. Benitez-Paez, E.M.Del Pulgar, et al., Gut microbiota, diet, and obesity-related disorders-the good, the bad, and the future challenges, Mol. Nutr. Food Res. 61 (2017). https://doi.org/10.1002/mnfr.201600252
DOI Google Scholar
[4]

R. Sender, S. Fuchs, R. Milo, Are we really vastly outnumbered? Revisiting the ratio of bacterial to host cells in humans, Cell 164 (2016) 337-340. https://doi.org/10.1016/j.cell.2016.01.013
DOI Google Scholar
[5]

P.B. Eckburg, E.M. Bik, C.N. Bernstein, et al., Diversity of the human intestinal microbial flora, Science 308 (2005) 1635-1638. https://doi.org/10.1126/science.1110591
DOI Google Scholar
[6]

P. Lapebie, V. Lombard, E. Drula, et al., Bacteroidetes use thousands of enzyme combinations to break down glycans, Nat. Commun. 10 (2019) 2043. https://doi.org/10.1038/s41467-019-10068-5
DOI Google Scholar
[7]

D.W. Cockburn, N.M. Koropatkin, Polysaccharide degradation by the intestinal microbiota and its influence on human health and disease, J. Mol. Biol. 428 (2016) 3230-3252. https://doi.org/10.1016/j.jmb.2016.06.021
DOI Google Scholar
[8]

S. Rakoff-Nahoum, K.R. Foster, L.E. Comstock, The evolution of cooperation within the gut microbiota, Nature 533 (2016) 255-259. https://doi.org/10.1038/nature17626
DOI Google Scholar
[9]

M. Mendis, E.C. Martens, S. Simsek, How fine structural differences of xylooligosaccharides and arabinoxylooligosaccharides regulate differential growth of bacteroides species, J. Agric. Food Chem. 66 (2018) 8398-8405. https://doi.org/10.1021/acs.jafc.8b01263
DOI Google Scholar
[10]

N. Terrapon, V. Lombard, H.J. Gilbert, et al., Automatic prediction of polysaccharide utilization loci in Bacteroidetes species, Bioinformatics 31 (2015) 647-655. https://doi.org/10.1093/bioinformatics/btu716
DOI Google Scholar
[11]

Q. Fang, J. Hu, Q. Nie, et al., Effects of polysaccharides on glycometabolism based on gut microbiota alteration, Trends Food Sci. Technol. 92 (2019) 65-70. https://doi.org/10.1016/j.tifs.2019.08.015
DOI Google Scholar
[12]

D.A. Muniz Pedrogo, M.D. Jensen, C.T.Van Dyke, et al., Gut microbial carbohydrate metabolism hinders weight loss in overweight adults undergoing lifestyle intervention with a volumetric diet, Mayo Clin. Proc. 93 (2018) 1104-1110. https://doi.org/10.1016/j.mayocp.2018.02.019
DOI Google Scholar
[13]

N.L. Zitomersky, M.J. Coyne, L.E. Comstock, Longitudinal analysis of the prevalence, maintenance, and IgA response to species of the order Bacteroidales in the human gut, Infect. Immun. 79 (2011) 2012-2020. https://doi.org/10.1128/iai.01348-10
DOI Google Scholar
[14]

R. Munoz, R. Rossello-Mora, R. Amann, Revised phylogeny of Bacteroidetes and proposal of sixteen new taxa and two new combinations including Rhodothermaeota phyl. nov, Syst. Appl. Microbiol. 39 (2016) 281-296. https://doi.org/10.1016/j.syapm.2016.04.004
DOI Google Scholar
[15]

I.B. Jeffery, D.B. Lynch, P.W. O'Toole, Composition and temporal stability of the gut microbiota in older persons, ISME J. 10 (2016) 170-182. https://doi.org/10.1038/ismej.2015.88
DOI Google Scholar
[16]

J. Qin, R. Li, J. Raes, et al., A human gut microbial gene catalogue established by metagenomic sequencing, Nature 464 (2010) 59-65. https://doi.org/10.1038/nature08821
DOI Google Scholar
[17]

S. Rakoff-Nahoum, M.J. Coyne, L.E. Comstock, An ecological network of polysaccharide utilization among human intestinal symbionts, Curr. Biol. 24 (2014) 40-49. https://doi.org/10.1016/j.cub.2013.10.077
DOI Google Scholar
[18]

K.G. Roelofs, M.J. Coyne, R.R. Gentyala, et al., Bacteroidales secreted antimicrobial proteins target surface molecules necessary for gut colonization and mediate competition in vivo, mBio 7 (2016) e01055-16. https://doi.org/10.1128/mbio.01055-16
DOI Google Scholar
[19]

M. Chatzidaki-Livanis, M.J. Coyne, K.G. Roelofs, et al., Gut symbiont bacteroides fragilis secretes a eukaryotic-like ubiquitin protein that mediates intraspecies antagonism, mBio 8 (2017) e01902-17. https://doi.org/10.1128/mbio.01902-17
DOI Google Scholar
[20]

M. Yin, Z. Yan, X. Li, Architecture of type Ⅵ secretion system membrane core complex, Cell Res. 29 (2019) 251-253. https://doi.org/10.1038/s41422-018-0130-7
DOI Google Scholar
[21]

E.A. Groisman, Feedback control of two-component regulatory systems, Annu. Rev. Microbiol. 70 (2016) 103-124. https://doi.org/10.1146/annurev-micro-102215-095331
DOI Google Scholar
[22]

M.A. Lonetto, K.L. Brown, K.E. Rudd, et al., Analysis of the Streptomyces coelicolor sigE gene reveals the existence of a subfamily of eubacterial RNA polymerase sigma factors involved in the regulation of extracytoplasmic functions, Proc. Natl. Acad. Sci. USA 91 (1994) 7573-7577. https://doi.org/10.1073/pnas.91.16.7573
DOI Google Scholar
[23]

E.C. Martens, R. Roth, J.E. Heuser, et al., Coordinate regulation of glycan degradation and polysaccharide capsule biosynthesis by a prominent human gut symbiont, J. Biol. Chem. 284 (2009) 18445-18457. https://doi.org/10.1074/jbc.M109.008094
DOI Google Scholar
[24]

J. Xu, M.K. Bjursell, J. Himrod, et al., A genomic view of the human-Bacteroides thetaiotaomicron symbiosis, Science 299 (2003) 2074-2076. https://doi.org/10.1126/science.1080029
DOI Google Scholar
[25]

Y.C. Chang, Y.H. Ching, C.C. Chiu, et al., TLR2 and interleukin-10 are involved in Bacteroides fragilis-mediated prevention of DSS-induced colitis in gnotobiotic mice, PLoS One 12 (2017) e0180025. https://doi.org/10.1371/journal.pone.0180025
DOI Google Scholar
[26]

J.L. Chan, S. Wu, A.L. Geis, et al., Non-toxigenic Bacteroides fragilis (NTBF) administration reduces bacteria-driven chronic colitis and tumor development independent of polysaccharide A, Mucosal Immunol. 12 (2019) 164-177. https://doi.org/10.1038/s41385-018-0085-5
DOI Google Scholar
[27]

Y.K. Lee, P. Mehrabian, S. Boyajian, et al., The protective role of Bacteroides fragilis in a murine model of colitis-associated colorectal cancer, mSphere 3 (2018) e00587-18. https://doi.org/10.1128/mSphere.00587-18
DOI Google Scholar
[28]

Z. Li, H. Deng, Y. Zhou, et al., Bioluminescence imaging to track Bacteroides fragilis inhibition of Vibrio parahaemolyticus infection in mice, Front. Cell. Infect. Microbiol. 7 (2017) 170. https://doi.org/10.3389/fcimb.2017.00170
DOI Google Scholar
[29]

T.S. Stappenbeck, L.V. Hooper, J.I. Gordon, Developmental regulation of intestinal angiogenesis by indigenous microbes via Paneth cells, Proc. Natl. Acad. Sci. USA 99 (2002) 15451-15455. https://doi.org/10.1073/pnas.202604299
DOI Google Scholar
[30]

A.G. Wexler, W.B. Schofield, P.H. Degnan, et al., Human gut Bacteroides capture vitamin B12 via cell surface-exposed lipoproteins, eLife 7 (2018) e37138. https://doi.org/10.7554/eLife.37138
DOI Google Scholar
[31]

M.M. Wegorzewska, R.W.P. Glowacki, S.A. Hsieh, et al., Diet modulates colonic T cell responses by regulating the expression of a Bacteroides thetaiotaomicron antigen, Sci. Immunol. 4 (2019) eaau9079. https://doi.org/10.1126/sciimmunol.aau9079
DOI Google Scholar
[32]

P. Ulsemer, K. Toutounian, G. Kressel, et al., Impact of oral consumption of heat-treated Bacteroides xylanisolvens DSM 23964 on the level of natural TFα-specific antibodies in human adults, Benef. Microbes 7 (2016) 485-500. https://doi.org/10.3920/BM2015.0143
DOI Google Scholar
[33]

N. Yoshida, T. Emoto, T. Yamashita, et al., Bacteroides vulgatus and Bacteroides dorei reduce gut microbial lipopolysaccharide production and inhibit atherosclerosis, Circulation 138 (2018) 2486-2498. https://doi.org/10.1161/CIRCULATIONAHA.118.033714
DOI Google Scholar
[34]

L. Garcia-Bayona, L.E. Comstock, Streamlined genetic manipulation of diverse Bacteroides and Parabacteroides isolates from the human gut microbiota, mBio 10 (2019) e01762-19. https://doi.org/10.1128/mBio.01762-19
DOI Google Scholar
[35]

Z.Z. Hamady, N. Scott, M.D. Farrar, et al., Treatment of colitis with a commensal gut bacterium engineered to secrete human TGF-beta1 under the control of dietary xylan, Inflamm. Bowel Dis. 17 (2011) 1925-1935. https://doi.org/10.1002/ibd.21565
DOI Google Scholar
[36]

J.Y. Yang, Y.S. Lee, Y. Kim, et al., Gut commensal Bacteroides acidifaciens prevents obesity and improves insulin sensitivity in mice, Mucosal Immunol. 10 (2017) 104-116. https://doi.org/10.1038/mi.2016.42
DOI Google Scholar
[37]

R.E. Ley, P.J. Turnbaugh, S. Klein, et al., Microbial ecology: human gut microbes associated with obesity, Nature 444 (2006) 1022-1023. https://doi.org/10.1038/4441022a
DOI Google Scholar
[38]

R.C. Kaplan, Z. Wang, M. Usyk, et al., Gut microbiome composition in the Hispanic Community Health Study/Study of Latinos is shaped by geographic relocation, environmental factors, and obesity, Genome Biol. 20 (2019) 219. https://doi.org/10.1186/s13059-019-1831-z
DOI Google Scholar
[39]

Y. Ren, Y. Bai, Z. Zhang, et al., The preparation and structure analysis methods of natural polysaccharides of plants and fungi: a review of recent development, Molecules 24 (2019) 3122. https://doi.org/10.3390/molecules24173122
DOI Google Scholar
[40]

E.C. Martens, H.C. Chiang, J.I. Gordon, Mucosal glycan foraging enhances fitness and transmission of a saccharolytic human gut bacterial symbiont, Cell Host Microbe 4 (2008) 447-457. https://doi.org/10.1016/j.chom.2008.09.007
DOI Google Scholar
[41]

K. Tamura, G.R. Hemsworth, G. Dejean, et al., Molecular mechanism by which prominent human gut Bacteroidetes utilize mixed-linkage beta-glucans, major health-promoting cereal polysaccharides, Cell Rep. 21 (2017) 417-430. https://doi.org/10.1016/j.celrep.2017.09.049
DOI Google Scholar
[42]

N.P. McNulty, M. Wu, A.R. Erickson, et al., Effects of diet on resource utilization by a model human gut microbiota containing Bacteroides cellulosilyticus WH2, a symbiont with an extensive glycobiome, PLoS Biol. 11 (2013) e1001637. https://doi.org/10.1371/journal.pbio.1001637
DOI Google Scholar
[43]

E.C. Martens, E.C. Lowe, H. Chiang, et al., Recognition and degradation of plant cell wall polysaccharides by two human gut symbionts, PLoS Biol. 9 (2011) e1001221. https://doi.org/10.1371/journal.pbio.1001221
DOI Google Scholar
[44]

Y. Cao, E.R. Rocha, C.J. Smith, Efficient utilization of complex N-linked glycans is a selective advantage for Bacteroides fragilis in extraintestinal infections, Proc. Natl. Acad. Sci. USA 111 (2014) 12901-12906. https://doi.org/10.1073/pnas.1407344111
DOI Google Scholar
[45]

J. Despres, E. Forano, P. Lepercq, et al., Xylan degradation by the human gut Bacteroides xylanisolvens XB1A(T) involves two distinct gene clusters that are linked at the transcriptional level, BMC Genomics 17 (2016) 326. https://doi.org/10.1186/s12864-016-2680-8
DOI Google Scholar
[46]

A.S. Tauzin, E. Laville, Y. Xiao, et al., Functional characterization of a gene locus from an uncultured gut Bacteroides conferring xylo-oligosaccharides utilization to Escherichia coli, Mol. Microbiol. 102 (2016) 579-592. https://doi.org/10.1111/mmi.13480
DOI Google Scholar
[47]

N.D. Schwalm III, E.A. Groisman, Navigating the gut buffet: control of polysaccharide utilization in Bacteroides spp, Trends Microbiol. 25 (2017) 1005-1015. https://doi.org/10.1016/j.tim.2017.06.009
DOI Google Scholar
[48]

Z. Zhang, Q. Liu, W.A. Hendrickson, Crystal structures of apparent saccharide sensors from histidine kinase receptors prevalent in a human gut symbiont, FEBS J. 281 (2014) 4263-4279. https://doi.org/10.1111/febs.12904
DOI Google Scholar
[49]

J.N. D'Elia, A.A. Salyers, Effect of regulatory protein levels on utilization of starch by Bacteroides thetaiotaomicron, J. Bacteriol. 178 (1996) 7180-7186. https://doi.org/10.1128/jb.178.24.7180-7186.1996
DOI Google Scholar
[50]

R.A. Luu, R.A. Schomer, C.N. Brunton, et al., Hybrid two-component sensors for identification of bacterial chemoreceptor function, Appl. Environ. Microbiol. 85 (2019) e01626-19. https://doi.org/10.1128/AEM.01626-19
DOI Google Scholar
[51]
V. Raghavan, E.C. Lowe, G.E. Townsend, 2nd, et al., Tuning transcription of nutrient utilization genes to catabolic rate promotes growth in a gut bacterium, Mol. Microbiol. 93 (2014) 1010-1025. https://doi.org/10.1111/mmi.12714
DOI
[52]

N.D. Schwalm, G.E. Townsend, E.A. Groisman, Prioritization of polysaccharide utilization and control of regulator activation in Bacteroides thetaiotaomicron, Mol. Microbiol. 104 (2017) 32-45. https://doi.org/10.1111/mmi.13609
DOI Google Scholar
[53]

N.T. Porter, A.S. Luis, E.C. Martens, Bacteroides thetaiotaomicron, Trends Microbiol. 26 (2018) 966-967. https://doi.org/10.1016/j.tim.2018.08.005
DOI Google Scholar
[54]

M.H. Foley, D.W. Cockburn, N.M. Koropatkin, The Sus operon: a model system for starch uptake by the human gut Bacteroidetes, Cell. Mol. Life Sci. 73 (2016) 2603-2617. https://doi.org/10.1007/s00018-016-2242-x
DOI Google Scholar
[55]

M.P. Bos, J. Tommassen, Biogenesis of the gram-negative bacterial outer membrane, Curr. Opin. Microbiol. 7 (2004) 610-616. https://doi.org/10.1016/j.mib.2004.10.011
DOI Google Scholar
[56]

H.H. Tuson, M.H. Foley, N.M. Koropatkin, et al., The starch utilization system assembles around stationary starch-binding proteins, Biophys. J. 115 (2018) 242-250. https://doi.org/10.1016/j.bpj.2017.12.015
DOI Google Scholar
[57]

M.H. Foley, E.C. Martens, N.M. Koropatkin, SusE facilitates starch uptake independent of starch binding in B. thetaiotaomicron, Mol. Microbiol. 108 (2018) 551-566. https://doi.org/10.1111/mmi.13949
DOI Google Scholar
[58]

R. Grinter, T. Lithgow, The crystal structure of the TonB-dependent transporter YncD reveals a positively charged substrate-binding site, Acta. Crystallogr. D Struct. Biol. 76 (2020) 484-495. https://doi.org/10.1107/S2059798320004398
DOI Google Scholar
[59]

D.N. Bolam, B. van den Berg, TonB-dependent transport by the gut microbiota: novel aspects of an old problem, Curr. Opin. Struct. Biol. 51 (2018) 35-43. https://doi.org/10.1016/j.sbi.2018.03.001
DOI Google Scholar
[60]

D.A. Ravcheev, A. Godzik, A.L. Osterman, et al., Polysaccharides utilization in human gut bacterium Bacteroides thetaiotaomicron: comparative genomics reconstruction of metabolic and regulatory networks, BMC Genomics 14 (2013) 873. https://doi.org/10.1186/1471-2164-14-873
DOI Google Scholar
[61]

M. Kitamura, M. Okuyama, F. Tanzawa, et al., Structural and functional analysis of a glycoside hydrolase family 97 enzyme from Bacteroides thetaiotaomicron, J. Biol. Chem. 283 (2008) 36328-36337. https://doi.org/10.1074/jbc.M806115200
DOI Google Scholar
[62]

R.E. Ley, M. Hamady, C. Lozupone, et al., Evolution of mammals and their gut microbes, Science 320 (2008) 1647-1651. https://doi.org/10.1126/science.1155725
DOI Google Scholar
[63]

M.H. Foley, G. Dejean, G.R. Hemsworth, et al., A cell-surface GH9 endo-glucanase coordinates with surface glycan-binding proteins to mediate xyloglucan uptake in the gut symbiont Bacteroides ovatus, J. Mol. Biol. 431 (2019) 981-995. https://doi.org/10.1016/j.jmb.2019.01.008
DOI Google Scholar
[64]

P. Joglekar, E.D. Sonnenburg, S.K. Higginbottom, et al., Genetic variation of the susc/susd homologs from a polysaccharide utilization locus underlies divergent fructan specificities and functional adaptation in Bacteroides thetaiotaomicron strains, mSphere 3 (2018) e00185-18. https://doi.org/10.1128/mSphereDirect.00185-18
DOI Google Scholar
[65]

D. Ndeh, A. Rogowski, A. Cartmell, et al., Complex pectin metabolism by gut bacteria reveals novel catalytic functions, Nature 544 (2017) 65-70. https://doi.org/10.1038/nature21725
DOI Google Scholar
[66]

D. Ndeh, A. Basle, H. Strahl, et al., Metabolism of multiple glycosaminoglycans by Bacteroides thetaiotaomicron is orchestrated by a versatile core genetic locus, Nat. Commun. 11 (2020) 646. https://doi.org/10.1038/s41467-020-14509-4
DOI Google Scholar
[67]

L. Kjellen, U. Lindahl, Specificity of glycosaminoglycan-protein interactions, Curr. Opin. Struct. Biol. 50 (2018) 101-108. https://doi.org/10.1016/j.sbi.2017.12.011
DOI Google Scholar
[68]

J.E. Ulmer, E.M. Vilen, R.B. Namburi, et al., Characterization of glycosaminoglycan (GAG) sulfatases from the human gut symbiont Bacteroides thetaiotaomicron reveals the first GAG-specific bacterial endosulfatase, J. Biol. Chem. 289 (2014) 24289-24303. https://doi.org/10.1074/jbc.M114.573303
DOI Google Scholar
[69]

A. Cartmell, E.C. Lowe, A. Basle, et al., How members of the human gut microbiota overcome the sulfation problem posed by glycosaminoglycans, Proc. Natl. Acad. Sci. USA 114 (2017) 7037-7042. https://doi.org/10.1073/pnas.1704367114
DOI Google Scholar
[70]

E.C. Lowe, A. Basle, M. Czjzek, et al., A scissor blade-like closing mechanism implicated in transmembrane signaling in a Bacteroides hybrid two-component system, Proc. Natl. Acad. Sci. USA 109 (2012) 7298-7303. https://doi.org/10.1073/pnas.1200479109
DOI Google Scholar
[71]

A. Rogowski, J.A. Briggs, J.C. Mortimer, et al., Glycan complexity dictates microbial resource allocation in the large intestine, Nat. Commun. 6 (2015) 7481. https://doi.org/10.1038/ncomms8481
DOI Google Scholar
[72]

V. Raghavan, E.A. Groisman, Species-specific dynamic responses of gut bacteria to a mammalian glycan, J. Bacteriol. 197 (2015) 1538-1548. https://doi.org/10.1128/JB.00010-15
DOI Google Scholar
[73]

J. Larsbrink, T.E. Rogers, G.R. Hemsworth, et al., A discrete genetic locus confers xyloglucan metabolism in select human gut Bacteroidetes, Nature 506 (2014) 498-502. https://doi.org/10.1038/nature12907
DOI Google Scholar
[74]

F. Cuskin, E.C. Lowe, M.J. Temple, et al., Human gut Bacteroidetes can utilize yeast mannan through a selfish mechanism, Nature 517 (2015) 165-169. https://doi.org/10.1038/nature13995
DOI Google Scholar
[75]

E.A. Bayer, R. Lamed, B.A. White, et al., From cellulosomes to cellulosomics, Chem. Rec. 8 (2008) 364-377. https://doi.org/10.1002/tcr.20160
DOI Google Scholar
[76]

L. Artzi, E.A. Bayer, S. Morais, Cellulosomes: bacterial nanomachines for dismantling plant polysaccharides, Nat. Rev. Microbiol. 15 (2017) 83-95. https://doi.org/10.1038/nrmicro.2016.164
DOI Google Scholar
[77]

N. Zeybek, R.A. Rastall, A.O. Buyukkileci, Utilization of xylan-type polysaccharides in co-culture fermentations of Bifidobacterium and Bacteroides species, Carbohydrate Polymers 236 (2020) 116076. https://doi.org/10.1016/j.carbpol.2020.116076
DOI Google Scholar
[78]

M.A. Mahowald, F.E. Rey, H. Seedorf, et al., Characterizing a model human gut microbiota composed of members of its two dominant bacterial phyla, Proc. Natl. Acad. Sci. USA 106 (2009) 5859-5864. https://doi.org/10.1073/pnas.0901529106
DOI Google Scholar
[79]

W. Elhenawy, M.O. Debelyy, M.F. Feldman, Preferential packing of acidic glycosidases and proteases into Bacteroides outer membrane vesicles, mBio 5 (2014) e00909-00914. https://doi.org/10.1128/mBio.00909-14
DOI Google Scholar
[80]

E.J. Jones, C. Booth, S. Fonseca, et al., The uptake, trafficking, and biodistribution of Bacteroides thetaiotaomicron generated outer membrane vesicles, Front. Microbiol. 11 (2020) 57. https://doi.org/10.3389/fmicb.2020.00057
DOI Google Scholar
[81]

S. Zhao, C. Jang, J. Liu, et al., Dietary fructose feeds hepatic lipogenesis via microbiota-derived acetate, Nature 579 (2020) 586-591. https://doi.org/10.1038/s41586-020-2101-7
DOI Google Scholar
[82]

A. Esposito, S. Tamburini, L. Triboli, et al., Insights into the genome structure of four acetogenic bacteria with specific reference to the Wood-Ljungdahl pathway, Microbiologyopen 8 (2019) e938. https://doi.org/10.1002/mbo3.938
DOI Google Scholar
[83]

P. Louis, H.J. Flint, Formation of propionate and butyrate by the human colonic microbiota, Environ. Microbiol. 19 (2017) 29-41. https://doi.org/10.1111/1462-2920.13589
DOI Google Scholar
[84]

T.K. Bjarnadottir, D.E. Gloriam, S.H. Hellstrand, et al., Comprehensive repertoire and phylogenetic analysis of the G protein-coupled receptors in human and mouse, Genomics 88 (2006) 263-273. https://doi.org/10.1016/j.ygeno.2006.04.001
DOI Google Scholar
[85]

A. Koh, F. de Vadder, P. Kovatcheva-Datchary, et al., From dietary fiber to host physiology: short-chain fatty acids as key bacterial metabolites, Cell 165 (2016) 1332-1345. https://doi.org/10.1016/j.cell.2016.05.041
DOI Google Scholar
[86]

A.J. Brown, S.M. Goldsworthy, A.A. Barnes, et al., The orphan G protein-coupled receptors GPR41 and GPR43 are activated by propionate and other short chain carboxylic acids, J. Biol. Chem. 278 (2003) 11312-11319. https://doi.org/10.1074/jbc.M211609200
DOI Google Scholar
[87]

L. Macia, J. Tan, A.T. Vieira, et al., Metabolite-sensing receptors GPR43 and GPR109A facilitate dietary fibre-induced gut homeostasis through regulation of the inflammasome, Nat. Commun. 6 (2015) 6734. https://doi.org/10.1038/ncomms7734
DOI Google Scholar
[88]

Y. Tian, Q. Xu, L. Sun, et al., Short-chain fatty acids administration is protective in colitis-associated colorectal cancer development, J. Nutr. Biochem. 57 (2018) 103-109. https://doi.org/10.1016/j.jnutbio.2018.03.007
DOI Google Scholar
[89]

N. Singh, A. Gurav, S. Sivaprakasam, et al., Activation of Gpr109a, receptor for niacin and the commensal metabolite butyrate, suppresses colonic inflammation and carcinogenesis, Immunity 40 (2014) 128-139. https://doi.org/10.1016/j.immuni.2013.12.007
DOI Google Scholar
[90]

W. Yang, T. Yu, X. Huang, et al., Intestinal microbiota-derived short-chain fatty acids regulation of immune cell IL-22 production and gut immunity, Nat. Commun. 11 (2020) 4457. https://doi.org/10.1038/s41467-020-18262-6
DOI Google Scholar
[91]

M. Thangaraju, G. Cresci, S. Itagaki, et al., Sodium-coupled transport of the short chain fatty acid butyrate by SLC5A8 and its relevance to colon cancer, J. Gastrointest. Surg. 12 (2008) 1773-1781. https://doi.org/10.1007/s11605-008-0573-0
DOI Google Scholar
[92]

P.V. Chang, L. Hao, S. Offermanns, et al., The microbial metabolite butyrate regulates intestinal macrophage function via histone deacetylase inhibition, Proc. Natl. Acad. Sci. USA 111 (2014) 2247-2252. https://doi.org/10.1073/pnas.1322269111
DOI Google Scholar
[93]

J. Park, M. Kim, S.G. Kang, et al., Short-chain fatty acids induce both effector and regulatory T cells by suppression of histone deacetylases and regulation of the mTOR-S6K pathway, Mucosal Immunol. 8 (2015) 80-93. https://doi.org/10.1038/mi.2014.44
DOI Google Scholar
[94]

F. Chen, W. Yang, X. Huang, et al., Neutrophils promote amphiregulin production in intestinal epithelial cells through TGF-beta and contribute to intestinal homeostasis, J. Immunol. 201 (2018) 2492-2501. https://doi.org/10.4049/jimmunol.1800003
DOI Google Scholar
[95]

G. Desalegn, O. Pabst, Inflammation triggers immediate rather than progressive changes in monocyte differentiation in the small intestine, Nat. Commun. 10 (2019) 3229. https://doi.org/10.1038/s41467-019-11148-2
DOI Google Scholar
[96]

P.M. Smith, M.R. Howitt, N. Panikov, et al., The microbial metabolites, short-chain fatty acids, regulate colonic Treg cell homeostasis, Science 341 (2013) 569-573. https://doi.org/10.1126/science.1241165
DOI Google Scholar
[97]

M.A. Vinolo, G.J. Ferguson, S. Kulkarni, et al., SCFAs induce mouse neutrophil chemotaxis through the GPR43 receptor, PLoS One 6 (2011) e21205. https://doi.org/10.1371/journal.pone.0021205
DOI Google Scholar
[98]

Y. Furusawa, Y. Obata, S. Fukuda, et al., Commensal microbe-derived butyrate induces the differentiation of colonic regulatory T cells, Nature 504 (2013) 446-450. https://doi.org/10.1038/nature12721
DOI Google Scholar
[99]

M.R. Fernando, A. Saxena, J.L. Reyes, et al., Butyrate enhances antibacterial effects while suppressing other features of alternative activation in IL-4-induced macrophages, Am. J. Physiol. Gastrointest. Liver Physiol. 310 (2016) G822-831. https://doi.org/10.1152/ajpgi.00440.2015
DOI Google Scholar
[100]

K. Atarashi, T. Tanoue, K. Oshima, et al., Treg induction by a rationally selected mixture of Clostridia strains from the human microbiota, Nature 500 (2013) 232-236. https://doi.org/10.1038/nature12331
DOI Google Scholar
[101]

W. Wu, M. Sun, F. Chen, et al., Microbiota metabolite short-chain fatty acid acetate promotes intestinal IgA response to microbiota which is mediated by GPR43, Mucosal Immunol. 10 (2017) 946-956. https://doi.org/10.1038/mi.2016.114
DOI Google Scholar
[102]

H. Fan, Z. Chen, R. Lin, et al., Bacteroides fragilis strain ZY-312 defense against Cronobacter sakazakii-induced necrotizing enterocolitis in vitro and in a neonatal rat model, mSystems 4 (2019) e00305-19. https://doi.org/10.1128/mSystems.00305-19
DOI Google Scholar
[103]

W. Zhang, B. Zhu, J. Xu, et al., Bacteroides fragilis protects against antibiotic-associated diarrhea in rats by modulating intestinal defenses, Front. Immunol. 9 (2018) 1040. https://doi.org/10.3389/fimmu.2018.01040
DOI Google Scholar
[104]

M. Delday, I. Mulder, E.T. Logan, et al., Bacteroides thetaiotaomicron ameliorates colon inflammation in preclinical models of crohn's disease, Inflamm. Bowel Dis. 25 (2019) 85-96. https://doi.org/10.1093/ibd/izy281
DOI Google Scholar
[105]

H. Tan, J. Zhao, H. Zhang, et al., Novel strains of Bacteroides fragilis and Bacteroides ovatus alleviate the LPS-induced inflammation in mice, Appl. Microbiol. Biotechnol. 103 (2019) 2353-2365. https://doi.org/10.1007/s00253-019-09617-1
DOI Google Scholar
[106]

V. Bagenholm, S.K. Reddy, H. Bouraoui, et al., Galactomannan catabolism conferred by a polysaccharide utilization locus of Bacteroides ovatus: enzyme synergy and crystal structure of a beta-mannanase, J. Biol. Chem. 292 (2017) 229-243. https://doi.org/10.1074/jbc.M116.746438
DOI Google Scholar
[107]

M. Centanni, S.M. Carnachan, T.J. Bell, et al., Utilization of complex pectic polysaccharides from New Zealand plants (Tetragonia tetragonioides and Corynocarpus laevigatus) by gut bacteroides species, J. Agric. Food Chem. 67 (2019) 7755-7764. https://doi.org/10.1021/acs.jafc.9b02429
DOI Google Scholar
[108]

A.S. Luis, J. Briggs, X. Zhang, et al., Dietary pectic glycans are degraded by coordinated enzyme pathways in human colonic Bacteroides, Nat. Microbiol. 3 (2018) 210-219. https://doi.org/10.1038/s41564-017-0079-1
DOI Google Scholar
[109]

G.P. Rodriguez-Castano, M.R. Dorris, X. Liu, et al., Bacteroides thetaiotaomicron starch utilization promotes quercetin degradation and butyrate production by Eubacterium ramulus, Front. Microbiol. 10 (2019) 1145. https://doi.org/10.3389/fmicb.2019.01145
DOI Google Scholar
[110]

K. Mardo, T. Visnapuu, H. Vija, et al., A highly active endo-levanase bt1760 of a dominant mammalian gut commensal Bacteroides thetaiotaomicron cleaves not only various bacterial levans, but also levan of timothy grass, PLoS One 12 (2017) e0169989. https://doi.org/10.1371/journal.pone.0169989
DOI Google Scholar
[111]

J. Chen, C.S. Robb, F. Unfried, et al., Alpha- and beta-mannan utilization by marine Bacteroidetes, Environ. Microbiol. 20 (2018) 4127-4140. https://doi.org/10.1111/1462-2920.14414
DOI Google Scholar
[112]

A. Cartmell, J. Munoz-Munoz, J.A. Briggs, et al., A surface endogalactanase in Bacteroides thetaiotaomicron confers keystone status for arabinogalactan degradation, Nat. Microbiol. 3 (2018) 1314-1326. https://doi.org/10.1038/s41564-018-0258-8
DOI Google Scholar
[113]

A. Benitez-Paez, E.M. Gomez Del Pulgar, Y. Sanz, The glycolytic versatility of Bacteroides uniformis CECT 7771 and its genome response to oligo and polysaccharides, Front. Cell. Infect. Microbiol. 7 (2017) 383. https://doi.org/10.3389/fcimb.2017.00383
DOI Google Scholar
Publication history
Copyright
Acknowledgements
Rights and permissions

Publication history

Received: 08 December 2020
Revised: 30 December 2020
Accepted: 24 January 2021
Published: 02 June 2022
Issue date: September 2022

Copyright

© 2022 Beijing Academy of Food Sciences.

Acknowledgements

The financial supports are coming from the National Science Fund for Distinguished Young Scholars of China (31825020).

Rights and permissions

This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).

Return