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Open Access

Ameliorative effects of Lactobacillus fermentum isolated from individuals following vegan, omnivorous and high-meat diets on ulcerative colitis in mice

Qingsong Zhanga,bWei Xiaoa,bLeilei Yua,bFengwei Tiana,bJianxin Zhaoa,b( )Hao Zhanga,b,c,dWei Chena,b,cQixiao Zhaia,b( )
State Key Laboratory of Food Science and Technology, Jiangnan University, Wuxi 214122, China
School of Food Science and Technology, Jiangnan University, Wuxi 214122, China
National Engineering Research Center for Functional Food, Jiangnan University, Wuxi 214122, China
Wuxi Translational Medicine Research Center and Jiangsu Translational Medicine Research Institute Wuxi Branch, Wuxi 214122, China

Peer review under responsibility of Tsinghua University Press.

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Abstract

Lactobacillus spp. can be beneficial for the prevention or treatment of ulcerative colitis (UC). In this study, 153 participants who followed vegan, omnivorous, or high-meat diet were recruited. Compositional analysis of the Lactobacillus community in feces revealed that Lactobacillus fermentum strains were significantly affected by diet. Administration of mixed L. fermentum strains from vegans significantly improved inflammation compared to that from omnivores and high-meat consumers, as evidenced by a significant reduction in colonic tissue damage, improvement in inflammatory cytokines, enhanced expression of ZO-1, occludin, and claudin-3, and a significant increase in short chain fatty acids concentration. The effect of a single strain of L. fermentum was similar to that of a mixed strains of L. fermentum group. Genomic analysis suggested that L. fermentum strains from the guts of vegans possessed a higher prevalence of genes involved in carbohydrate catabolism than those from the guts of omnivores and high-meat eaters. In particular, the ME2 gene is involved in the biosynthesis of acetate, a compound considered to possess anti-inflammatory properties. In conclusion, this study indicates strain-specific differences in the ability of L. fermentum strains to alleviate UC in mice, influenced by habitual diets.

References

[1]

P. Hindryckx, G. Novak, N.C. Vande, et al., Review article: dose optimisation of infliximab for acute severe ulcerative colitis, Aliment. Pharmacol. Ther. 45 (2017) 617-630. https://doi.org/10.1111/apt.13913.

[2]

N. Goyal, A. Rana, A. Ahlawat, et al., Animal models of inflammatory bowel disease: a review, Inflammopharmacology 22 (2014) 219-233. https://doi.org/10.1007/s10787-014-0207-y.

[3]

K. Tripathi, J.D. Feuerstein, New developments in ulcerative colitis: latest evidence on management, treatment, and maintenance, Drugs Context 8 (2019) 1-11. https://doi.org/10.7573/dic.212572.

[4]

H. Khalili, S.S.M. Chan, P. Lochhead, et al., The role of diet in the aetiopathogenesis of inflammatory bowel disease, Nat. Rev. Gastroenterol. Hepatol. 15 (2018) 525-535. https://doi.org/10.1038/s41575-018-0022-9.

[5]

J. Pieczynska, A. Prescha, K. Zabłocka-Słowińska, et al., Occurrence of dietary risk factors in inflammatory bowel disease: influence on the nutritional status of patients in clinical remission, Adv. Clin. Exp. Med. 28 (2019) 587-592. https://doi.org/10.17219/acem/78590.

[6]

S.L. Jowett, C.J. Seal, M.S. Pearce, et al., Influence of dietary factors on the clinical course of ulcerative colitis: a prospective cohort study, Gut 53 (2004) 1479-1484. https://doi.org/10.1136/gut.2003.024828.

[7]

M. Chiba, K. Nakane, T. Tsuji, et al., Relapse prevention by plant-based diet incorporated into induction therapy for ulcerative colitis: a single-group trial, Perm. J. 23 (2019) 18-220. https://doi.org/10.7812/TPP/18-220.

[8]

E.A. Franzosa, A. Sirota-Madi, J. Avila-Pacheco, et al., Gut microbiome structure and metabolic activity in inflammatory bowel disease, Nat. Microbiol. 4 (2019) 293-305. https://doi.org/10.1038/s41564-018-0306-4.

[9]

S. Guandalini, N. Sansotta, Probiotics in the treatment of inflammatory bowel disease, Adv. Exp. Med. Biol. 1125 (2019) 101-107. https://doi.org/10.1007/5584_2018_319.

[10]

J. Shi, Q. Xie, Y. Yue, et al., Gut microbiota modulation and anti-inflammatory properties of mixed lactobacilli in dextran sodium sulfate-induced colitis in mice, Food Funct. 12 (2021) 5130-5143. https://doi.org/10.1039/d1fo00317h.

[11]

W.K. Kim, D.H. Han, Y.J. Jang, et al., Alleviation of DSS-induced colitis via Lactobacillus acidophilus treatment in mice, Food Funct. 12 (2021) 340-350. https://doi.org/10.1039/d0fo01724h.

[12]

P. Yu, C. Ke, J. Guo, et al., Lactobacillus alleviates colitis by inhibiting LPS-mediated NF-κB activation and ameliorates DSS-induced gut microbiota dysbiosis, Front. Immunol. 11 (2020) 575173. https://doi.org/10.3389/fimmu.2020.575173.

[13]

G. Wang, S. Huang, S. Cai, et al., Lactobacillus reuteri ameliorates intestinal inflammation and modulates gut microbiota and metabolic disorders in dextran sulfate sodium-induced colitis in mice, Nutrients 12 (2020) 2298. https://doi.org/10.3390/nu12082298.

[14]

X. Dou, L. Qiao, J. Chang, et al., Lactobacillus casei ATCC 393 and it’s metabolites alleviate dextran sulphate sodium-induced ulcerative colitis in mice through the NLRP3-(Caspase-1)/IL-1β pathway, Food Funct. 12 (2021) 12022-12035. https://doi.org/10.1039/d1fo02405a.

[15]

Y.J. Jang, W.K. Kim, D.H. Han, et al., Lactobacillus fermentum species ameliorate dextran sulfate sodium-induced colitis by regulating the immune response and altering gut microbiota, Gut Microbes 10 (2019) 696-711. https://doi.org/10.1080/19490976.2019.1589281.

[16]

J.L. Sonnenburg, F. Bäckhed, Diet-microbiota interactions as moderators of human metabolism, Nature 535 (2016) 56-64. https://doi.org/10.1038/nature18846.

[17]

F.D. Vadder, P. Kovatcheva-Datchary, C. Zitoun, et al., Microbiota-produced succinate improves glucose homeostasis via intestinal gluconeogenesis, Cell Metab. 24 (2016) 151-157. https://doi.org/10.1016/j.cmet.2016.06.013.

[18]

A. Nogal, A.M. Valdes, C. Menni, The role of short-chain fatty acids in the interplay between gut microbiota and diet in cardio-metabolic health, Gut Microbes 13 (2021) 1-24. https://doi.org/10.1080/19490976.2021.1897212.

[19]

G. Precup, D.C. Vodnar, Gut Prevotella as a possible biomarker of diet and its eubiotic versus dysbiotic roles: a comprehensive literature review, Br. J. Nut. 122 (2019) 131-140. https://doi.org/10.1017/S0007114519000680.

[20]

P.B. Stege, J. Hordijk, S.A. Shetty, et al., Impact of long-term dietary habits on the human gut resistome in the Dutch population, Sci. Rep. 12 (2022) 1892. https://doi.org/10.1038/s41598-022-05817-4.

[21]

N. Mann, Y. Pirotta, S. O’Connell, et al., Fatty acid composition of habitual omnivore and vegetarian diets, Lipids 41 (2006) 637-646. https://doi.org/10.1007/s11745-006-5014-9.

[22]

M. Xie, M. Pan, Y. Jiang, et al., groEL gene-based phylogenetic analysis of Lactobacillus species by high-throughput sequencing, Genes 10 (2019) 530. https://doi.org/10.3390/genes10070530.

[23]

Y. Zhao, L. Yu, F. Tian, et al., An optimized culture medium to isolate Lactobacillus fermentum strains from the human intestinal tract, Food Funct. 12 (2021) 6740-6754. https://doi.org/10.1039/d1fo00209k.

[24]

D. Luongo, L. Treppiccione, A. Sorrentino, et al., Immune-modulating effects in mouse dendritic cells of lactobacilli and bifidobacteria isolated from individuals following omnivorous, vegetarian and vegan diets, Cytokine 97 (2017) 141-148. https://doi.org/10.1016/j.cyto.2017.06.007.

[25]

Y. Chen, Y. Chen, C. Stanton, et al., Dose-response efficacy and mechanisms of orally administered CLA-producing Bifidobacterium breve CCFM683 on DSS-induced colitis in mice, Food Funct. 75 (2020) 952. https://doi.org/10.3390/nu15081952.

[26]

C. Wang, S. Li, K. Hong, et al., The roles of different Bacteroides fragilis strains in protecting against DSS-induced ulcerative colitis and related functional genes, Food Funct. 12 (2021) 8300-8313. https://doi.org/10.1039/d1fo00875g.

[27]

L. Wang, M. Pan, D. Li, et al., Metagenomic insights into the effects of oligosaccharides on the microbial composition of cecal contents in constipated mice, J. Funct. Foods 38 (2017) 486-496. https://doi.org/10.1016/j.jff.2017.09.045.

[28]

Y. Zhao, J. Wu, J. Yang, et al., PGAP: pan-genomes analysis pipeline, Bioinformatics 28 (2012) 416-418. https://doi.org/10.1093/bioinformatics/btr655.

[29]

K. Liu, T. Warnow, Large-scale multiple sequence alignment and tree estimation using SATé, Methods Mol. Biol. (2014) 219-244. https://doi.org/10.1007/978-1-62703-646-7_15.

[30]

C. Tong, Q. Chen, L. Zhao, et al., Identification and characterization of long intergenic noncoding RNAs in bovine mammary glands, BMC Genomics 18 (2017) 468. https://doi.org/10.1186/s12864-017-3858-4.

[31]

J. Zou, C. Liu, S. Jiang, et al., Cross talk between gut microbiota and intestinal mucosal immunity in the development of ulcerative colitis, Infect. Immun. 89 (2021) e00014-21. https://doi.org/10.1128/IAI.00014-21.

[32]

A.D. Kostic, R.J. Xavier, D. Gevers, The microbiome in inflammatory bowel disease: current status and the future ahead, Gastroenterology 146 (2014) 1489-1499. https://doi.org/10.1053/j.gastro.2014.02.009.

[33]

J.J. Faith, J.F. Colombel, J.I. Gordon, Identifying strains that contribute to complex diseases through the study of microbial inheritance, PNAS 112 (2015) 633-640. https://doi.org/10.1073/pnas.1418781112.

[34]

S. Greenblum, R. Carr, E. Borenstein, Extensive strain-level copy-number variation across human gut microbiome species, Cell 160 (2015) 583-594. https://doi.org/10.1016/j.cell.2014.12.038.

[35]

A.B. Shevtsov, A.R. Kushugulova, I.K. Tynybaeva, et al., Identification of phenotypically and genotypically related Lactobacillus strains based on nucleotide sequence analysis of the groEL, rpoB, rplB, and 16S rRNA genes, Mikrobiologiia 80 (2011) 659-668. https://doi.org/10.1134/S0026261711050134.

[36]

C.M. Dobson, B. Chaban, H. Deneer, et al., Lactobacillus casei, Lactobacillus rhamnosus, and Lactobacillus zeae isolates identified by sequence signature and immunoblot phenotype, Can. J Microbiol. 50 (2004) 482-488. https://doi.org/10.1139/w04-044.

[37]

P. Cronin, S.A. Joyce, P.W. O’Toole, et al., Dietary fibre modulates the gut microbiota, Nutrients 13 (2021) 1655. https://doi.org/10.3390/nu13051655.

[38]

E.A. Losno, K. Sieferle, F.J.A. Perez-Cueto, et al., Vegan diet and the gut microbiota composition in healthy adults, Nutrients 13 (2021) 2402. https://doi.org/10.3390/nu13072402.

[39]

V. Bunešová, M. Joch, S. Musilová, et al., Bifidobacteria, lactobacilli, and short chain fatty acids of vegetarians and omnivores, Sci. Agric. Bohem. 48 (2017) 47-54. https://doi.org/10.1515/sab-2017-0007.

[40]

L. Su, F. Ma, Z. An, et al., The Metabolites of Lactobacillus fermentum F-B9-1 relieved dextran sulfate sodium-induced experimental ulcerative colitis in mice, Front. Microbiol. 13 (2022) 865925. https://doi.org/10.3389/fmicb.2022.865925.

[41]

Z. Chen, L. Yi, Y. Pan, et al., Lactobacillus fermentum ZS40 ameliorates inflammation in mice with ulcerative colitis induced by dextran sulfate sodium, Front. Pharmacol. 12 (2021) 700217. https://doi.org/10.3389/fphar.2021.700217.

[42]

A. Rodriguez-Nogales, F. Algieri, J. Garrido-Mesa, et al., Differential intestinal anti-inflammatory effects of Lactobacillus fermentum and Lactobacillus salivarius in DSS mouse colitis: impact on microRNAs expression and microbiota composition, Mol. Nutr. Food Res. 61 (2017). https://doi.org/10.1002/mnfr.201700144.

[43]

H. Schmitz, C. Barmeyer, M. Fromm, et al., Altered tight junction structure contributes to the impaired epithelial barrier function in ulcerative colitis, Gastroenterology 116 (1999) 301-309. https://doi.org/10.1016/s0016-5085(99)70126-5.

[44]

L. Peran, D. Camuesco, M. Comalada, et al., Lactobacillus fermentum, a probiotic capable to release glutathione, prevents colonic inflammation in the TNBS model of rat colitis, Int. J. Colorectal Dis. 21 (2006) 737-746. https://doi.org/10.1007/s00384-005-0773-y.

[45]

F. Li, H. Huang, F. Zhu, et al., A mixture of Lactobacillus fermentum HFY06 and arabinoxylan ameliorates dextran sulfate sodium-induced acute ulcerative colitis in mice, J. Inflamm. Res. 14 (2021) 6575-6585. https://doi.org/10.2147/JIR.S344695.

[46]

C.I. Daien, J. Tan, R. Audo, et al., Gut-derived acetate promotes B10 cells with antiinflammatory effects, JCI Insight 6 (2021) e144156. https://doi.org/10.1172/jci.insight.144156.

[47]

H.J. Flint, K.P. Scott, P. Louis, et al., The role of the gut microbiota in nutrition and health, Nat. Rev. Gastroenterol. Hepatol. 9 (2012) 577-589. https://doi.org/10.1038/nrgastro.2012.156.

[48]

F. De Vadder, P. Kovatcheva-Datchary, D. Goncalves, et al., Microbiota-generated metabolites promote metabolic benefits via gut-brain neural circuits, Cell 156 (2014) 84-96. https://doi.org/10.1016/j.cell.2013.12.016.

[49]

S. De Santis, E. Cavalcanti, M. Mastronardi, et al., Nutritional keys for intestinal barrier modulation, Front. Immunol. 6 (2015) 612. https://doi.org/10.3389/fimmu.2015.00612.

[50]

A.N. Thorburn, L. Macia, C.R. Mackay, Diet, metabolites, and “Westernlifestyle” inflammatory diseases, Immunity 40 (2014) 833-842. https://doi.org/10.1016/j.immuni.2014.05.014.

[51]

F. Blachier, F. Mariotti, J.F. Huneau, et al., Effects of amino acid-derived luminal metabolites on the colonic epithelium and physiopathological consequences, Amino Acids 33 (2007) 547-562. https://doi.org/10.1007/s00726-006-0477-9.

[52]

A. Koh, F.D. 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.

[53]

Z. Zhang, H. Zhang, T. Chen, et al., Regulatory role of short-chain fatty acids in inflammatory bowel disease, Cell Commun. Signal. 20 (2022) 64. https://doi.org/10.1186/s12964-022-00869-5.

[54]

P. Louis, G.L. Hold, H.J. Flint, The gut microbiota, bacterial metabolites and colorectal cancer, Nat. Rev. Microbiol. 12 (2014) 661-672. https://doi.org/10.1038/nrmicro3344.

[55]

F.E. Rey, J.J. Faith, J. Bain, et al., Dissecting the in vivo metabolic potential of two human gut acetogens, J. Biol. Chem. 285 (2010) 22082-22090. https://doi.org/10.1074/jbc.M110.117713.

[56]

K.M. Maslowski, A.T. Vieira, A. Ng, et al., Regulation of inflammatory responses by gut microbiota and chemoattractant receptor GPR43, Nature 461 (2009) 1282-1286. https://doi.org/10.1038/nature08530.

Food Science and Human Wellness
Pages 3181-3192
Cite this article:
Zhang Q, Xiao W, Yu L, et al. Ameliorative effects of Lactobacillus fermentum isolated from individuals following vegan, omnivorous and high-meat diets on ulcerative colitis in mice. Food Science and Human Wellness, 2024, 13(6): 3181-3192. https://doi.org/10.26599/FSHW.2023.9250005

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Received: 15 October 2022
Revised: 01 March 2023
Accepted: 09 May 2023
Published: 18 December 2024
© 2024 Beijing Academy of Food Sciences. Publishing services by Tsinghua University Press.

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

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