Journal Home > Volume 11 , Issue 2

People are increasingly aware of the role of vegetarian diets in modulating human gut microbial abundance and intestinal physiology. A plant-based diet is thought to benefit host health by contributing to establish a diverse and stable microbiome. In addition, microbe-derived metabolites of specific nutrients known to be abundant in vegetarian diets (such as indigestible carbohydrates, arginine, and others) are important to promote effective intestinal immune responses, maintain intestinal barrier function, and protect against pathogens. This review explores the characteristics of the gut microbiome formed by vegetarian diets and the effects of diet-associated nutrients on intestinal microbial abundance. The interactions between the microbe-derived metabolites of vegetarian diet-associated nutrients and intestinal physiology are also discussed.


menu
Abstract
Full text
Outline
About this article

Effects of vegetarian diet-associated nutrients on gut microbiota and intestinal physiology

Show Author's information Wei Xiaoa,bQingsong Zhanga,bLeilei Yua,b,cFengwei Tiana,b,cWei Chena,b,d,eQixiao Zhaia,b,c( )
State Key Laboratory of Food Science and Technology, Jiangnan University, Wuxi 214122, China
School of Food Science and Technology, Jiangnan University, Wuxi 214122, China
International Joint Research Laboratory for Probiotics at Jiangnan University, Wuxi 214122 China
National Engineering Research Center for Functional Food, Jiangnan University, Wuxi 214122, China
Beijing Innovation Center of Food Nutrition and Human Health, Beijing Technology and Business University (BTBU), Beijing 100048, China

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

Abstract

People are increasingly aware of the role of vegetarian diets in modulating human gut microbial abundance and intestinal physiology. A plant-based diet is thought to benefit host health by contributing to establish a diverse and stable microbiome. In addition, microbe-derived metabolites of specific nutrients known to be abundant in vegetarian diets (such as indigestible carbohydrates, arginine, and others) are important to promote effective intestinal immune responses, maintain intestinal barrier function, and protect against pathogens. This review explores the characteristics of the gut microbiome formed by vegetarian diets and the effects of diet-associated nutrients on intestinal microbial abundance. The interactions between the microbe-derived metabolites of vegetarian diet-associated nutrients and intestinal physiology are also discussed.

Keywords: Gut microbiota, Vegetarian diet, Microbial metabolites, Intestinal physiology

References(110)

[1]

M.J. Orlich, N.S. Pramil, J. Sabaté, et al., Vegetarian dietary patterns and mortality in adventist health study 2, JAMA Intern. Med. 173 (2013) 1230-1238. https://doi.org/10.1001/jamainternmed.2013.6473.

[2]

P. Clary, D. Tom, H. Inge, et al., Comparison of nutritional quality of the vegan, vegetarian, semi-vegetarian, pesco-vegetarian and omnivorous diet, Nutrients 6 (2014) 1318-1332. https://doi.org/10.3390/nu6031318.

[3]

V. Melina, W. Craig, S. Levin, Position of the academy of nutrition and dietetics: vegetarian diets, J. Acad. Nutr. Diet. 116 (2016) 1970-1980. https://doi.org/10.1016/j.jand.2016.09.025.

[4]

H. Kahleova, M. Matoulek, H. Malinska, et al., Vegetarian diet improves insulin resistance and oxidative stress markers more than conventional diet in subjects with type 2 diabetes, Diabetic Med. 28 (2011) 549-559. https://doi.org/10.1111/j.1464-5491.2010.03209.x.

[5]

H.J. Zhang, P. Han, S.Y. Sun, et al., Attenuated associations between increasing BMI and unfavorable lipid profiles in Chinese Buddhist vegetarians, Asia Pac. J. Clin. Nutr. 22 (2013) 249-256. https://doi.org/10.3390/nu6062131.

[6]

L.T. Le, J. Sabate, Beyond meatless, the health effects of vegan diets: findings from the Adventist cohorts, Nutrients 6 (2014) 2131-2147. https://doi.org/10.3390/nu6062131.

[7]

E.H. Haddad, L. S Berk, J.D. Kettering, et al., Dietary intake and biochemical, hematologic, and immune status of vegans compared with nonvegetarians, Am. J. Clin. Nutr. 70 (1999) 586s-593s. https://doi.org/10.1093/ajcn/70.3.586s.

[8]

T.H.T. Chiu, H.Y. Huang, Y.F. Chiu, et al., Taiwanese vegetarians and omnivores: dietary composition, prevalence of diabetes and IFG, PLoS One 9 (2014) e88547. https://doi.org/10.1371/journal.pone.0088547.

[9]

N. Burkholder-Cooley, S. Rajaram, E. Haddad, et al., Comparison of polyphenol intakes according to distinct dietary patterns and food sources in the Adventist Health Study-2 cohort, Brit. J. Nutr. 115 (2016) 2162-2169. https://doi.org/10.1017/S0007114516001331.

[10]

K. Jaceldo-Siegl, D. Lütjohann, R. Sirirat, et al., Variations in dietary intake and plasma concentrations of plant sterols across plant based diets among North American adults, Mol. Nutr. Food Res. 61 (2017) 1600828. https://doi.org/10.1002/mnfr.201600828.

[11]

R.C. Travis, N.E. Allen, P.N. Appleby, et al., A prospective study of vegetarianism and isoflavone intake in relation to breast cancer risk in British women, Int. J. Cancer 122 (2008) 705-710. https://doi.org/10.1002/ijc.23141.

[12]

F.D. Filippis, E. Pasolli, A. Tett, et al., Distinct genetic and functional traits of human intestinal Prevotella copri strains are associated with different habitual diets, Cell Host Microbe. 25 (2019) 444-453. https://doi.org/10.1016/j.chom.2019.01.004.

[13]

L.A. David, C.F. Maurice, R.N. Carmody, et al., Diet rapidly and reproducibly alters the human gut microbiome, Nature 505 (2014) 559-563. https://doi.org/10.1038/nature12820.

[14]

S. Ruengsomwong, O. La-Ongkham, J. Jiang, et al., Microbial community of healthy thai vegetarians and non-vegetarians, their core gut microbiota, and pathogen risk, J. Microbiol. Biotechn. 26 (2016) 1723-1735. https://doi.org/10.4014/jmb.1603.03057.

[15]

M.S. Kim, S.S. Hwang, E.J. Park, et al., Strict vegetarian diet improves the risk factors associated with metabolic diseases by modulating gut microbiota and reducing intestinal inflammation, Env. Microbiol. Rep. 5 (2013) 765-775. https://doi.org/10.1111/1758-2229.12079.

[16]

R. Pawlak, P. Vos, S. Shahab-Ferdows, et al., Vitamin B-12 content in breast milk of vegan, vegetarian, and nonvegetarian lactating women in the United States, Am. J. Clin. Nutr. 108 (2018) 525-531. https://doi.org/10.1093/ajcn/nqy104.

[17]

G. Sebastiani, A.H. Barbero, C. Borrás-Novell, et al., The effects of vegetarian and vegan diet during pregnancy on the health of mothers and offspring, Nutrients 11 (2019) 557. https://doi.org/10.3390/nu11030557.

[18]

H. Hayashi, M. Sakamoto, Y. Benno, Fecal microbial diversity in a strict vegetarian as determined by molecular analysis and cultivation, Microbiol. Immunol. 46 (2002) 819-831. https://doi.org/10.1111/j.1348-0421.2002. tb02769.x.

[19]

J. Kabeerdoss, R.S. Devi, R.R. Mary, et al., Faecal microbiota composition in vegetarians: comparison with omnivores in a cohort of young women in southern India, Br. J. Nutr. 108 (2012) 953-957. https://doi.org/10.1017/ S0007114511006362.

[20]

R. Hemalatha, A.C. Ouwehand, M.T. Saarinen, et al., Bifidobacteria, Lactobacilli, and short chain fatty acids of vegetarians and omnivores, Scientia Agriculturae Bohemica 48 (2017) 47-54. https://doi.org/10.1515/sab-2017-0007.

[21]

C. Zhang, B. Andrea, K. Cai, et al., Impact of a 3-months vegetarian diet on the gut microbiota and immune repertoire, Front. Immunol. 9 (2018) 908. https://doi.org/10.3389/fimmu.2018.00908.

[22]

H.L. Barrett, L.F. Gomez-Arango, S.A. Wilkinson, et al., A vegetarian diet is a major determinant of gut microbiota composition in early pregnancy, Nutrients 10 (2018) 890. https://doi.org/10.3390/nu10070890.

[23]

S. Ruengsomwong, Y. Korenori, N. Sakamoto, et al., Senior Thai fecal microbiota comparison between vegetarians and non-vegetarians using PCRDGGE and real-time PCR, J. Microbiol. Biotechn. 24 (2014) 1026-1033. https://doi.org/10.4014/jmb.1310.10043.

[24]

J. Zimmer, B. Lange, J.S. Frick, et al., A vegan or vegetarian diet substantially alters the human colonic faecal microbiota, Eur. J. Clin. Nutr. 66 (2012) 53-60. https://doi.org/10.1038/ejcn.2011.141.

[25]

N.S. Klimenko, A.V. Tyakht, A.S. Popenko, et al., Microbiome responses to an uncontrolled short-term diet intervention in the frame of the Citizen Science Project, Nutrients 10 (2018) 576. https://doi.org/10.3390/nu10050576.

[26]

G.D. Wu, J. Chen, C. Hoffmann, et al., Linking long-term dietary patterns with gut microbial enterotypes, Science 334 (2011) 105-108. https://doi.org/10.1126/science.1208344.

[27]

E. Federici, R. Prete, C. Lazzi, et al., Bacterial composition, genotoxicity, and cytotoxicity of fecal samples from individuals consuming omnivorous or vegetarian diets, Front. Microbiol. 8 (2017) 300. https://doi.org/10.10.3389/fmicb.2017.00300.

[28]

B.B. Matijašić, T. Obermajer, L. Lipoglavšek, et al., Association of dietary type with fecal microbiota in vegetarians and omnivores in Slovenia, Eur. J. Nutr. 53 (2014) 1051-1064. https://doi.org/10.1007/s00394-013-0607-6.

[29]

I. Ferrocin, R.D. Cagno, M.D. Angelis, et al., Fecal microbiota in healthy subjects following omnivore, vegetarian and vegan diets: culturable populations and rRNA DGGE profiling, PLoS One 10 (2015) e0128669. https://doi.org/10.1371/journal.pone.0128669.

[30]

C. Losasso, E.M. Eckert, E. Mastrorilli, et al., Assessing the influence of vegan, vegetarian and omnivore oriented westernized dietary styles on human gut microbiota: a cross sectional study, Front. Microbiol. 9 (2018) 317. https://doi.org/10.3389/fmicb.2018.00317.

[31]

F.D. Filippis, N. Pellegrini, L. Vannini, et al., Association of dietary type with fecal microbiota and short chain fatty acids in vegans and omnivores, J. Int. Soc. Microbiota. 1 (2016) 1. https://doi.org/10.1136/gutjnl-2015-309957.

[32]

M. Zinöcker, I. Lindseth, The Western diet–microbiome-host interaction and its role in metabolic disease, Nutrients 10 (2018) 365. https://doi.org/10.3390/nu10030365.

[33]

K. Oliphant, E. Allen-Vercoe, Macronutrient metabolism by the human gut microbiome: major fermentation by-products and their impact on host health, Microbiome 7 (2019) 1-15. https://doi.org/10.1186/s40168-019-0704-8.

[34]

E.P. Halmos, C.T. Christophersen, A.R. Bird, et al., Diets that differ in their FODMAP content alter the colonic luminal microenvironment, Gut 64 (2015) 93-100. https://doi.org/10.1136/gutjnl-2014-307264.

[35]

A. Cotillard, S.P. Kennedy, L.C. Kong, et al., Dietary intervention impact on gut microbial gene richness, Nature 500 (2013) 585. https://doi.org/10.1038/ nature12480.

[36]

S.H. Duncan, A. Belenguer, G. Holtrop, et al., Reduced dietary intake of carbohydrates by obese subjects results in decreased concentrations of butyrate and butyrate-producing bacteria in feces, Appl. Environ. Microbiol. 73 (2007) 1073-1078. https://doi.org/10.1128/AEM.02340-06.

[37]

B.S. Drasar, J.S. Crowther, P. Goddard, et al., The relation between diet and the gut microflora in man, P. Nutr. Soc. 32 (1973) 49-52. https://doi.org/10.1079/pns19730014.

[38]

F. Fava, R. Gitau, B.A. Griffin, et al., The type and quantity of dietary fat and carbohydrate alter faecal microbiome and short-chain fatty acid excretion in a metabolic syndrome 'at-risk' population, Int. J. Obesity 37 (2013) 216-223. https://doi.org/10.1038/ijo.2012.33.

[39]

H.J. Urwin, E.A. Miles, P.S. Noakes, et al., Effect of salmon consumption during pregnancy on maternal and infant faecal microbiota, secretory IgA and calprotectin, Brit. J. Nutr. 111 (2014) 773-784. https://doi.org/10.1017/S0007114513003097.

[40]

D.J. Hentges, B.R. Maier, G.C. Burton, et al., Effect of a high-beef diet on the fecal bacterial flora of humans, Cancer Res. 37 (1977) 568-571. https://doi.org/10.1016/0091-7435(77)90008-1.

[41]

D. Świątecka, A. Narbad, K.P. Ridgway, et al., The study on the impact of glycated pea proteins on human intestinal bacteria, Int. J. Food Microbiol. 145 (2011) 267-272. https://doi.org/10.1016/j.ijfoodmicro.2011.01.002.

[42]

Z. Lv, Y. Wang, T. Yang, et al., Vitamin A deficiency impacts the structural segregation of gut microbiota in children with persistent diarrhea, J. Clin. Biochem. Nutr. 59 (2016) 15-148. https://doi.org/10.3164/jcbn.15-148.

[43]

M.C. Hibberd, M. Wu, D.A. Rodionov, et al., The effects of micronutrient deficiencies on bacterial species from the human gut microbiota, Sci. Transl. Med. 9 (2017) eaal4069. https://doi.org/10.1126/scitranslmed.aal4069.

[44]

S. Mandal, K.M. Godfrey, D. McDonald, et al., Fat and vitamin intakes during pregnancy have stronger relations with a pro-inflammatory maternal microbiota than does carbohydrate intake, Microbiome 4 (2016) 55. https://doi.org/10.1186/s40168-016-0200-3.

[45]

A. Chaplin, P. Parra, S. Laraichi, et al., Calcium supplementation modulates gut microbiota in a prebiotic manner in dietary obese mice, Mol. Nutr. Food Res. 60 (2016) 468-480. https://doi.org/10.1002/mnfr.201500480.

[46]

T. Clavel, M. Fallani, P. Lepage, et al., Isoflavones and functional foods alter the dominant intestinal microbiota in postmenopausal women, J. Nutr. 135 (2005) 2786-2792. https://doi.org/10.1089/jmf.2005.8.560

[47]

A. Klinde, Q. Shen, S. Heppel, et al., Impact of increasing fruit and vegetables and flavonoid intake on the human gut microbiota, Food Funct. 7 (2016) 1788-1796. https://doi.org/10.1039/c5fo01096a.

[48]

X. Tzouni, A. Rodriguez-Mateos, J. Vulevic, et al., Prebiotic evaluation of cocoa-derived flavanols in healthy humans by using a randomized, controlled, double-blind, crossover intervention study, Am. J. Clin. Nutr. 93 (2011) 62-72. https://doi.org/10.3945/ajcn.110.000075.

[49]

I. Moreno-Indias, L. Sánchez-Alcoholado, P. Pérez-Martínez, et al., Red wine polyphenols modulate fecal microbiota and reduce markers of the metabolic syndrome in obese patients, Food Funct. 7 (2016) 1775-1787. https://doi.org/10.1039/c5fo00886g.

[50]

K. Wang, X. Jin, Q. Li, et al., Propolis from different geographic origins decreases intestinal inflammation and Bacteroides spp. populations in a model of DSS-induced colitis, Mol. Nutr. Food Res. 62 (2018) 1800080. https://doi.org/10.1002/mnfr.201800080.

[51]

S. Baumgartne, R.P. Mensink, E.D. Smet, et al., Effects of plant stanol ester consumption on fasting plasma oxy (phyto) sterol concentrations as related to fecal microbiota characteristics, J. Steroid Biochem. 169 (2017) 46-53. https://doi.org/10.1016/j.jsbmb.2016.02.029.

[52]

L. Song, Y. Li, D. Qu, et al., The regulatory effects of phytosterol esters (PSEs) on gut flora and faecal metabolites in rats with NAFLD, Food Funct. 11 (2020) 977-991. https://doi.org/10.1039/c9fo01570a.

[53]

J. Slavin, Fiber and prebiotics: mechanisms and health benefits, Nutrients 5 (2013) 1417-1435. https://doi.org/10.3390/nu5041417.

[54]

A. Costabile, A. Klinder, F. Fava, et al., Whole-grain wheat breakfast cereal has a prebiotic effect on the human gut microbiota: a double-blind, placebo-controlled, crossover study, Brit. J. Nutr. 99 (2008) 110-120. https://doi.org/10.1017/S0007114507793923.

[55]

A.L. Carvalho-Wells, K. Helmolz, C. Nodet, et al., Determination of the in vivo prebiotic potential of a maize-based whole grain breakfast cereal: a human feeding study, Brit. J. Nutr. 104 (2010) 1353-1356. https://doi.org/10.1017/S0007114510002084.

[56]

S.H. Kim, D.H. Lee, D. Meyer, Supplementation of infant formula with native inulin has a prebiotic effect in formula-fed babies, Asia Pac. J. Clin. Nutr. 16 (2007) 172-177. https://doi.org/10.6133/apjcn.2007.16.1.22.

[57]

Z. Shan, P. Steenhout, K. Dong, et al., Nutritional support of pediatric patients with cancer consuming an enteral formula with fructooligosaccharides, Nutr. Res. 26 (2006) 154-162. https://doi.org/10.1016/j.nutres.2006.04.001.

[58]

S. Bartosc, E.J. Woodmansey, J.C.M. Paterson, et al., Microbiological effects of consuming a synbiotic containing Bifidobacterium bifidum, Bifidobacterium lactis, and oligofructose in elderly persons, determined by real-time polymerase chain reaction and counting of viable bacteria, Clin. Infect. Dis. 40 (2005) 28-37. https://doi.org/10.1086/426027.

[59]

A. Cebeci, C. Gürakan, Properties of potential probiotic Lactobacillus plantarum strains, Food Microbiol. 20 (2003) 511-518. https://doi.org/10.1016/S0740-0020(02)00174-0.

[60]

H. Kaplan, R.W. Hutkins, Fermentation of fructooligosaccharides by lactic acid bacteria and bifidobacteria, Appl. Environ. Microbiol. 66 (2000) 2682-2684. https://doi.org/10.1016/j.ijom.2009.11.012.

[61]

G.C.J. Abell, C.M. Cooke, C.N. Bennett, et al., Phylotypes related to Ruminococcus bromii are abundant in the large bowel of humans and increase in response to a diet high in resistant starch, FEMS Microbiol. Ecol. 66 (2008) 505-515. https://doi.org/10.1111/j.1574-6941.2008.00527.x.

[62]

A.W. Walker, J. Ince, S.H. Duncan, et al., Dominant and diet-responsive groups of bacteria within the human colonic microbiota, ISME J. 5 (2011) 220. https://doi.org/10.1038/ismej.2010.118.

[63]

T.V. Maier, M. Lucio, L.H. Lee, et al., Impact of dietary resistant starch on the human gut microbiome, metaproteome, and metabolome, MBio. 8 (2017) e01343-17. https://doi.org/10.1128/mBio.01343-17.

[64]

P. Morales, S. Fujio, P. Navarrete, et al., Impact of dietary lipids on colonic function and microbiota: an experimental approach involving orlistatinduced fat malabsorption in human volunteers, Clin. Transl. Gastroen. 7 (2016) e161. https://doi.org/10.1038/ctg.2016.20.

[65]

V.M. Monnier, Bacterial enzymes that can deglycate glucose-and fructosemodified lysine, Biochem. J. 392 (2005) e1-3. https://doi.org/10.10.1042/BJ20051625.

[66]

A. Kaulmann, T. Bohn, Bioactivity of polyphenols: preventive and adjuvant strategies toward reducing inflammatory bowel diseases-promises, perspectives, and pitfalls, Oxid. Med. Cell Longev. 2016 (2016) 9346470. https://doi.org/10.1155/2016/9346470.

[67]

M.C. Theilmann, Y.J. Goh, K.F. Nielsen, et al., Lactobacillus acidophilus metabolizes dietary plant glucosides and externalizes their bioactive phytochemicals, MBio. 8 (2017) e01421-17. https://doi.org/10.1128/mBio.01421-17.

[68]

G. Dingeo, A. Brito, H. Samouda, et al., Phytochemicals as modifiers of gut microbial communities, Food Funct. 11 (2020) 8444-8471. https://doi.org/10.1039/d0fo01483d.

[69]

H. Lee, G. Ko, New perspectives regarding the antiviral effect of vitamin A on norovirus using modulation of gut microbiota, Gut Microbes. 8 (2017) 616-620. https://doi.org/10.1080/19490976.2017.1353842.

[70]

C. Zhang, A. Björkman, K. Cai, et al., Impact of a 3-months vegetarian diet on the gut microbiota and immune repertoire, Front Immunol. 9 (2018) 908. https://doi.org/10.3389/fimmu.2018.00908.

[71]

C. Michaudel, H. Sokol, The gut microbiota at the service of immunometabolism, Cell Metab. 32 (2020) 514-523. https://doi.org/10.1016/ j.cmet.2020.09.004.

[72]

C. Martin, A. Augustin, Food safety and health, Engineering 6 (2020) 391- 392. https://doi.org/10.doi.org/10.1016/j.eng.2020.01.010.

[73]

E. Bailón, M. Cueto-Sola, P. Utrilla, et al., Butyrate in vitro immunemodulatory effects might be mediated through a proliferationrelated induction of apoptosis, Immunobiology 215 (2010) 863-873. https://doi.org/10.1016/j.imbio.2010.01.001.

[74]

Y. Furusaw, 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.

[75]

G.T. Macfarlane, S. Macfarlane, Fermentation in the human large intestine: its physiologic consequences and the potential contribution of prebiotics, J. Clin. Gastroenterol. 45 (2011) S120-S127. https://doi.org/10.1097/ MCG.0b013e31822fecfe.

[76]

M.R. Clausen, P. Mortensen, Kinetic studies on colonocyte metabolism of short chain fatty acids and glucose in ulcerative colitis, Gut 37 (1995) 684-689. https://doi.org/10.1136/gut.37.5.684.

[77]

T. Ishikawa, F. Nanjo, Dietary cycloinulooligosaccharides enhance intestinal immunoglobulin A production in mice, Biosci. Biotech. Bioch. 73 (2009) 677-682. https://doi.org/10.1271/bbb.80733.

[78]

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.

[79]

S. Tedelind, F. Westberg, M. Kjerrulf, et al., Anti-inflammatory properties of the short-chain fatty acids acetate and propionate: a study with relevance to inflammatory bowel disease, World J. Gastroenterol. 13 (2007) 2826. https://doi.org/10.3748/wjg.v13.i20.2826.

[80]

D. Bajic, A. Niemann, A.K. Hillmer, et al., Gut microbiota derived propionate regulates the expression of Reg3 mucosal lectins and ameliorates experimental colitis in mice, J. Crohns Colitis 14 (2020) 1462-1472. https://doi.org/10.1093/ecco-jcc/jjaa065.

[81]

L.C. Tong, Y. Wang, Z.B. Wang, et al., Propionate ameliorates dextran sodium sulfate-induced colitis by improving intestinal barrier function and reducing inflammation and oxidative stress, Front. Pharmacol. 7 (2016) 253. https://doi.org/10.3389/fphar.2016.00253.

[82]

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.

[83]

C.J. Kelly, L. Zheng, E.L. Campbell, et al., Crosstalk between microbiotaderived short-chain fatty acids and intestinal epithelial HIF augments tissue barrier function, Cell Host Microbe. 17 (2015) 662-671. https://doi.org/10.1016/j.chom.2015.03.005.

[84]

N.D. Mathewson, R. Jenq, A.V. Mathew, et al., Gut microbiome–derived metabolites modulate intestinal epithelial cell damage and mitigate graft-versushost disease, Nat. Immunol. 17 (2016) 505-513. https://doi.org/10.1038/ni.3400.

[85]

L. Wrzosek, S. Miquel, M.L. Noordine, et al., Bacteroides thetaiotaomicron and Faecalibacterium prausnitzii influence the production of mucus glycans and the development of goblet cells in the colonic epithelium of a gnotobiotic model rodent, BMC Biology 11 (2013) 1-13. https://doi.org/10.1186/1741- 7007-11-61.

[86]

M. Shan, M. Gentile, J.R. Yeiser, et al., Mucus enhances gut homeostasis and oral tolerance by delivering immunoregulatory signals, Science 342 (2013) 447-453. https://doi.org/10.1126/science.1237910.

[87]

S.H. Duncan, P. Louis, J.M. Thomson, et al., The role of pH in determining the species composition of the human colonic microbiota, Environ. Microbiol. 11 (2009) 2112-2122. https://doi.org/10.1111/j.1462-2920.2009.01931.x.

[88]
H.J. Flint, P. Louis, K.P. Scott, et al., Commensal bacteria in health and disease, in virulence mechanisms of bacterial pathogens, 4th edition. American Society of Microbiology (2007) 101-115. https://doi.org/10.1128/9781555815851.ch8.
[89]

F. Rivera-Chávez, L.F. Zhang, F. Faber, et al., Depletion of butyrateproducing Clostridia from the gut microbiota drives an aerobic luminal expansion of Salmonella, Cell Host Microbe. 19 (2016) 443-454. https://doi.org/10.1016/j.chom.2016.03.004.

[90]

M.X. Byndloss, E.E. Olsan, F. Rivera-Chávez, et al., Microbiota-activated PPAR-γ signaling inhibits dysbiotic Enterobacteriaceae expansion, Science 357 (2017) 570-575. https://doi.org/10.1126/science.aam9949.

[91]

J. Schulthess, S. Pandey, M. Capitani, et al., The short chain fatty acid butyrate imprints an antimicrobial program in macrophages, Immunity 50 (2019) 432-445. https://doi.org/10.1016/j.immuni.2018.12.018.

[92]

C.C. Hung, C.D. Garner, J.M. Slauch, et al., The intestinal fatty acid propionate inhibits Salmonella invasion through the post-translational control of HilD, Mol. Microbiol. 87 (2013) 1045-1060. https://doi.org/10.1111/ mmi.12149.

[93]

T. Watanabe, H. Nishio, T. Tanigawa, et al., Probiotic Lactobacillus casei strain Shirota prevents indomethacin-induced small intestinal injury: involvement of lactic acid, Am. J. Physiol-Gastr. L. 297 (2009) G506-G513. https://doi.org/10.1152/ajpgi.90553.

[94]

C. Iraporda, D.E. Romanin, M. Rumbo, et al., The role of lactate on the immunomodulatory properties of the nonbacterial fraction of kefir, Food Res. Int. 62 (2014) 247-253. https://doi.org/10.1016/j.foodres.2014.03.003.

[95]

C. Iraporda, A. Errea, D.E. Romanin, et al., Lactate and short chain fatty acids produced by microbial fermentation downregulate proinflammatory responses in intestinal epithelial cells and myeloid cells, Immunobiology 220 (2015) 1161-1169. https://doi.org/10.1016/j.imbio.2015.06.004.

[96]

Y.S. Lee, T.Y. Kim, Y. Kim, et al., Microbiota-derived lactate accelerates intestinal stem-cell-mediated epithelial development, Cell Host Microbe. 24 (2018) 833-846. https://doi.org/10.1016/j.chom.2018.11.002.

[97]

N. Morita, E. Umemoto, S. Fujita, et al., GPR31-dependent dendrite protrusion of intestinal CX3CR1+ cells by bacterial metabolites, Nature 566 (2019) 110-114. https://doi.org/10.1038/s41586-019-0884-1.

[98]

M. Veldhoen, V. Brucklacher-Waldert, Dietary influences on intestinal immunity, Nat. Rev. Immunol. 12 (2012) 696. https://doi.org/10.1038/nri3299.

[99]

M. Grizotte-Lake, G. Zhong, K. Duncan, et al., Commensals suppress intestinal epithelial cell retinoic acid synthesis to regulate interleukin-22 activity and prevent microbial dysbiosis, Immunity 49 (2018) 1103-1115. https://doi.org/10.1016/j.immuni.2018.11.018.

[100]

B. Mouillé, S. Delpal, C. Mayeur, et al., Inhibition of human colon carcinoma cell growth by ammonia: a non-cytotoxic process associated with polyamine synthesis reduction, BBA-GEN Subjects 1624 (2003) 88-97. https://doi.org/10.1016/j.bbagen.2003.09.014.

[101]

R. Kibe, S. Kurihara, Y. Sakai, et al., Upregulation of colonic luminal polyamines produced by intestinal microbiota delays senescence in mice, Sci. Rep. 4 (2014) 4548. https://doi.org/10.1038/srep04548.

[102]

G. Haskó, D.G. Kuhel, A. Marton, et al., Spermine differentially regulates the production of interleukin-12 p40 and interleukin-10 and suppresses the release of the T helper 1 cytokine interferon-γ, Shock 14 (2000) 144-149. https://doi.org/10.1097/00024382-200014020-00012.

[103]

J.P. Buts, N.D. Keyser, J. Kolanowski, et al., Maturation of villus and crypt cell functions in rat small intestine, Digest. Dis. Sci. 38 (1993) 1091-1098. https://doi.org/10.1007/BF01295726.

[104]

X. Guo, J.N. Rao, L. Liu, et al., Polyamines are necessary for synthesis and stability of occludin protein in intestinal epithelial cells, Am. J. Physiol-Gastr. L. 288 (2005) G1159-G1169. https://doi.org/10.1152/ajpgi.00407.2004.

[105]

J.N. Rao, N. Rathor, R. Zhuang, et al., Polyamines regulate intestinal epithelial restitution through TRPC1-mediated Ca2+ signaling by differentially modulating STIM1 and STIM2, Am. J. Physiol-Gastr. L. 303 (2012) C308-C317. https://doi.org/10.1152/ajpcell.00120.2012.a

[106]

D. Ríos-Covián, P. Ruas-Madiedo, A. Margolles, et al., Intestinal short chain fatty acids and their link with diet and human health, Front. Microbiol. 7 (2016) 185. https://doi.org/10.3389/fmicb.2016.00185.

[107]

M. Krajcovicova-Kudlackova, K. Babinska, M. Valachovicova, Health benefits and risks of plant proteins, Bratisl. Med. J. 106 (2005) 231.

[108]

K.A. Sharkey, P.L. Beck, D.M. McKay, Neuroimmunophysiology of the gut: advances and emerging concepts focusing on the epithelium, Nat. Rev. Gastro. Hepat. 15 (2018) 765-784. https://doi.org/10.1038/s41575-018-0051-4.

[109]

L.W. Peterson, D. Artis, Intestinal epithelial cells: regulators of barrier function and immune homeostasis, Nat. Rev. Immunol. 14 (2014) 141-153. https://doi.org/10.1038/nri3608.

[110]

G.R. Nicolas, P.V. Chang, Deciphering the chemical lexicon of hostgut microbiota interactions, Trends Pharmacol. Sci. 40 (2019) 430-445. https://doi.org/10.1016/j.tips.2019.04.006.

Publication history
Copyright
Rights and permissions

Publication history

Received: 24 December 2020
Revised: 30 January 2021
Accepted: 17 February 2021
Published: 25 November 2021
Issue date: March 2022

Copyright

© 2022 Beijing Academy of Food Sciences. Publishing services by Elsevier B.V. on behalf of KeAi Communications Co., Ltd.

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