Influence of diets on the composition of intestinal microflora and on immune processes in the human

Article Sidebar

pdf (Русский)
Published: Jul 21, 2024
DOI: https://doi.org/10.17072/1994-9952-2024-2-190-204
Keywords:
gut microflora vegan and vegetarian, ketogenic, gluten-free, Mediterranean diet low-chain carbohydrate diet (FODMAP) Western diet immune mechanisms

Main Article Content

Natalia A. Pravosudova
Penza State University, Penza, Russian Federation
Olga V. Marfina
Penza State University, Penza, Russian Federation
Viktor L. Melnikov
Penza State University, Penza, Russian Federation

Abstract

Diets, via the formation of a dominant microbial core, influence metabolic processes in the body, which determine changes in the individual's immune response. The work studies the influence of the main dietary regimes (vegan and vegetarian, ketogenic, gluten-free, Mediterranean diets, low FODMAP diet, Western diet) on the diversity and composition of the intestinal microflora. Vegans and vegetarians have a greater diversity of species from the Bacteroidetes group, an increase in the number of lactic acid bacteria such as Ruminococcus, E. rectale and Roseburia, and a decrease in the number of Clostridium and Enterococcus. This type of nutrition helps to enhance the protective properties of the intestines by increasing the number of bacteria that activate immune mechanisms. The ketogenic diet increases the number of Bacteroides and Akkermansia muciniphila, with a decrease in the number of Proteobacteria, Bifidobacteria, E. rectale, Dialister. As a result, the ketogenic diet alters the balance of pro- and anti-inflammatory mechanisms in the gut. A gluten-free diet causes a decrease in Bifidobacterium, Lactobacillus, Clostridium lituseburense, Faecalibacterium prausnitzii, Veillonellacea, Ruminicoccus bromii, Roseburia and an increase in the proportion of Enterobacteriacea (including Escherichia coli), Victivallaceae, Clostridiaceae and Coriobacteriaceae. This type of diet promotes the overgrowth of opportunistic microorganisms and weakens the host's defenses against infections and chronic inflammation. A diet low in short-chain carbohydrates (FODMAP) can lead to a decrease in the number of bifidobacteria, propionibacteria, F. prausnitzii, Akkermansia, Ruminococcus and an increase in the population of Clostridiaceae (Peptostreptococcus spp.) and, as a result, reduces the activity of immune mechanisms. The Western type of diet leads to a decrease in Bifidobacteria, Roseburia, Eubacterium, Ruminococcus, Lactobacillus, Prevotella and an increase in the number of Enterobacteria, Alistipes, Bacteroides. The Western type of diet, due to changes in the composition of normal microflora, increases the tendency towards obesity and weakening of protective properties. The Mediterranean diet leads to an increase in the concentration of F. prausnitzii, Bifidobacterium, Lactobacillus, Ruminococcus, Bacteroides and a decrease in the number of Clostridium, E. coli. This type of nutrition leads to a decrease in the number of opportunistic microorganisms and to the activation of immune mechanisms.

Article Details

How to Cite
Pravosudova Н. А., Marfina О. В. ., & Melnikov В. Л. . (2024). Influence of diets on the composition of intestinal microflora and on immune processes in the human. Bulletin of Perm University. Biology, (2), 190–204. https://doi.org/10.17072/1994-9952-2024-2-190-204
Issue
No. 2 (2024): Bulletin of Perm University. BIOLOGY
Section
Микробиология

License agreement

 

Author Biographies

Natalia A. Pravosudova, Penza State University, Penza, Russian Federation

PhD, Associate Professor of the Department of Microbiology, Epidemiology and Infectious Diseases

Olga V. Marfina, Penza State University, Penza, Russian Federation

PhD, Associate Professor of the Department of Microbiology, Epidemiology and Infectious Diseases

Viktor L. Melnikov, Penza State University, Penza, Russian Federation

Doctor of Medical Sciences, Head of the Department of Microbiology, Epidemiology and Infectious Diseases

References

Bukharin O.V., Ivanova E.V., Perunova N.B., Chainikova I.N. [The role of bifidobacteria in the formation of human immune homeostasis]. Žurnal microbiologii, èpidemiologii i immunobiologii. No. 6 (2015): pp. 98-104. (In Russ.).

Gabidullin Z.G. et al. [Interaction of bacteria of the Enterobacteriaceae family with antigen-presenting cells of the body’s immune system]. Medicinskij vestnik Baškortostana. V. 4, No. 5 (2009): pp. 78-86. (In Russ.).

Danilova N.A. et al. [Markers of dysbiosis in patients with ulcerative colitis and Crohn’s disease]. Tera-pevtičeskij arhiv. V. 91, No. 4 (2019): pp. 13-20. (In Russ.).

Ivashkin V.T., Zolnikova O.Yu. [Irritable Bowel Syndrome in Terms of Changes in the Microbiota]. Ros-sijskij žurnal gastroènterologii, gepatologii, koloproktologii. V. 29, No. 1 (2019): pp. 84-92. (In Russ.).

Karpeeva Yu.S., Novikova V.P., Khavkin A.I., Kovtun T.A., Makarkin D.V., Fedotova O.B. [Microbiota and human diseases: dietary correction]. Rossijskij vestnik perinatologii i pediatrii. V. 65, No. 5 (2020): pp. 116-125. (In Russ.).

Kozhevnikov A.A. et al. [Intestinal microbiota: modern ideas about species composition, functions and research methods]. RMŽ. V. 25, No. 17 (2017): pp. 1244-1247. (in Russ.).

Oganezova I.A. [Intestinal microbiota and immunity: immunomodulatory effects of Lactobacillus rham-nosus GG]. RMŽ. V. 26, No. 9 (2018): pp. 39-44. (in Russ.).

Stoma I.O. Mikrobiom v medicine [Microbiome in medicine. Guide for doctors]. Moscow, GEOTAR-Media Publ., 2020. 320 p. (In Russ.).

Afzaal M. et al. Human gut microbiota in health and disease: Unveiling the relationship. Frontiers in mi-crobiology. V. 13 (2022): pp. 999001. DOI: 10.3389/fmicb.2022.999001.

Almeida C. et al. The potential links between human gut microbiota and cardiovascular health and dis-ease-is there a gut-cardiovascular axis? Gut. V. 24 (2023): p. 25. DOI: 10.3389/fgstr.2023.1235126.

Ang Q.Y. et al. Ketogenic diets alter the gut microbiome resulting in decreased intestinal Th17 cells. Cell. V. 181, No. 6 (2020): pp. 1263-1275.e16. DOI: 10.1016/j.cell.2020.04.027.

Ansaldo E. et al. Akkermansia muciniphila induces intestinal adaptive immune responses during homeo-stasis. Science. V. 364 (2019): pp. 1179-1184. DOI: 10.1126/science.aaw7479.

Bäckhed F. et al. Structural requirements for TLR4-mediated LPS signalling: a biological role for LPS modifications. Microbes and infection. V. 5. No. 12 (2003): pp. 1057-1063. DOI: 10.1016/S1286-4579(03)00207-7.

Balty C. et al. Ruminococcin C, an anti-clostridial sactipeptide produced by a prominent member of the human microbiota Ruminococcus gnavus. Journal of Biological Chemistry. V. 294, No. 40 (2019): pp. 14512-14525. DOI: 10.1074/jbc.RA119.009416.

Bonder M.J. et al. The influence of a short-term gluten-free diet on the human gut microbiome. Genome medicine. V. 8 (2016): pp. 1-11. DOI: 10.1186/s13073-016-0295-y.

Chiumento S. et al. Ruminococcin C, a promising antibiotic produced by a human gut symbiont. Science advances. V. 5, No. 9 (2019): pp. eaaw9969. DOI: 10.1126/sciadv.aaw9969.

Christensen M.G., Damsgaard J., Fink-Jensen A. Use of ketogenic diets in the treatment of central nerv-ous system diseases: a systematic review. Nordic Journal of Psychiatry. V. 75, No. 1 (2021): pp. 1-8. DOI: 10.1080/08039488.2020.1795924.

Clemente-Suárez V.J. et al. Global Impacts of Western Diet and Its Effects on Metabolism and Health: A Narrative Review. Nutrients. V. 15. No. 12 (2023): pp. 2749. DOI: 10.3390/nu15122749

Cox M.A. et al. Short-chain fatty acids act as antiinflammatory mediators by regulating prostaglandin E(2) and cytokines. World journal of gastroenterology: WJG. V. 15, No. 44 (2009): pp. 5549-5557. DOI: 10.3748/wjg.15.5549.

Crost E.H. et al. Ruminococcus gnavus: friend or foe for human health. FEMS microbiology reviews. V. 47, No. 2 (2023): pp. fuad014. DOI: 10.1093/femsre/fuad014.

De Filippis F. et al. High-level adherence to a Mediterranean diet beneficially impacts the gut microbiota and associated metabolome. Gut. V. 65, No. 11 (2016): pp. 1812-1821. DOI: 10.1136/gutjnl-2015-309957.

De Palma G. et al. Effects of a gluten-free diet on gut microbiota and immune function in healthy adult human subjects. British journal of nutrition. V. 102, No. 8 (2009): pp. 1154-1160. DOI: 10.1017/S0007114509371767.

Depommier C. et al. Supplementation with Akkermansia muciniphila in overweight and obese human volunteers: a proof-of-concept exploratory study. Nature medicine. V. 25, No. 7 (2019): pp. 1096-1103. DOI: 10.1038/s41591-019-0495-2.

Donatella P., Aurelio C. Ketogenic diet and gut microbiota. PharmacologyOnLine. Special issue. V. 3 (2020): pp. 175-181.

Dunn K.A. et al. Early changes in microbial community structure are associated with sustained remission after nutritional treatment of pediatric Crohn's disease. Inflammatory bowel diseases. V. 22, No. 12 (2016): pp. 2853-2862. DOI: 10.1097/MIB.0000000000000956.

Everard A. et al. Cross-talk between Akkermansia muciniphila and intestinal epithelium controls diet-induced obesity. Proceedings of the national academy of sciences. V. 110, No. 22 (2013): pp. 9066-9071. DOI: 10.1073/pnas.1219451110

Gaboriau-Routhiau V. et al. The key role of segmented filamentous bacteria in the coordinated matura-tion of gut helper T cell responses. Immunity. V. 31, No. 4 (2009): pp. 677-689. DOI: 10.1016/j.immuni.2009.08.020.

Garcia-Mantrana I. et al. Shifts on gut microbiota associated to mediterranean diet adherence and spe-cific dietary intakes on general adult population. Frontiers in microbiology. V. 9 (2018): p. 890. DOI: 10.3389/fmicb.2018.00890.

Hiippala K. et al. The Potential of Gut Commensals in Reinforcing Intestinal Barrier Function and Alle-viating Inflammation. Nutrients. V. 10, No. 8 (2018): p. 988. DOI: 10.3390/nu10080988.

Hooper L.V. et al. Molecular analysis of commensal host-microbial relationships in the intestine. Science. V. 291, No. 5505 (2001): pp. 881-884. DOI: 10.1126/science.291.5505.881.

Hosoda S. et al. Revealing the microbial assemblage structure in the human gut microbiome using latent Dirichlet allocation. Microbiome. V. 8, No. 1 (2020): p. 95. DOI: 10.1186/s40168-020-00864-3.

Huuskonen J. et al. Regulation of microglial inflammatory response by sodium butyrate and short‐chain fatty acids. British journal of pharmacology. V. 141, No. 5 (2004): pp. 874-880. DOI: 10.1038/sj.bjp.0705682.

Jiang Y. et al. Acetyltransferase from Akkermansia muciniphila blunts colorectal tumourigenesis by re-programming tumour microenvironment. Gut. V. 72, No. 7 (2023): pp. 1308-1318. DOI: 10.1136/gutjnl-2022-327853.

Johnson J.L., Jones M.B., Cobb B.A. Polysaccharide A from the capsule of Bacteroides fragilis induces clonal CD4+ T cell expansion. Journal of Biological Chemistry. V. 290 No. 8 (2015): pp. 5007-5014. DOI: 10.1074/jbc.M114.621771.

Katiraei S. et al. Akkermansia muciniphila exerts lipid‐lowering and immunomodulatory effects without affecting neointima formation in hyperlipidemic APOE*3‐Leiden. CETP mice. Molecular nutrition & food re-search. V. 64, No. 15 (2020): pp. 1900732. DOI: 10.1002/mnfr.201900732.

Kopp W. How western diet and lifestyle drive the pandemic of obesity and civilization diseases. Diabe-tes, metabolic syndrome and obesity: targets and therapy. (2019): pp. 2221-2236. DOI: 10.2147/DMSO.S216791.

Kosinski C., Jornayvaz F.R. Effects of ketogenic diets on cardiovascular risk factors: evidence from an-imal and human studies. Nutrients. V. 9, No. 5 (2017): p. 517. DOI: 10.3390/nu9050517

Lécuyer E. et al. Segmented filamentous bacterium uses secondary and tertiary lymphoid tissues to in-duce gut IgA and specific T helper 17 cell responses. Immunity. V. 40, No. 4 (2014): pp. 608-620. DOI: 10.1016/j.immuni.2014.03.009.

Louis P. et al. Diversity of human colonic butyrate‐producing bacteria revealed by analysis of the butyr-yl‐CoA: acetate CoA‐transferase gene. Environmental microbiology. V. 12, No. 2 (2010): pp. 304-314. DOI: 10.1111/j.1462-2920.2009.02066.x.

Lozano C.P. et al. Associations of the Dietary Inflammatory Index with total adiposity and ectopic fat through the gut microbiota, LPS, and C-reactive protein in the Multiethnic Cohort–Adiposity Phenotype Study. The American Journal of Clinical Nutrition. V. 115, No. 5 (2022): pp. 1344-1356. DOI: 10.1093/ajcn/nqab398.

Lum G.R., Olson C.A., Hsiao E.Y. Emerging roles for the intestinal microbiome in epilepsy. Neurobiology of Disease. V. 135 (2020): pp. 104576. DOI: 10.1016/j.nbd.2019.104576.

Martens E.C. et al. Complex glycan catabolism by the human gut microbiota: the Bacteroidetes Sus-like paradigm. Journal of Biological Chemistry. V. 284, No. 37 (2009): pp. 24673-24677. DOI: 10.1074/jbc.R109.022848.

Martinez-Medina M., Garcia-Gil L.J. Escherichia coli in chronic inflammatory bowel diseases: An update on adherent invasive Escherichia coli pathogenicity. World journal of gastrointestinal pathophysiology. V. 5, No. 3 (2014): p. 213. DOI: 10.4291/wjgp.v5.i3.213.

Merra G. et al. Influence of mediterranean diet on human gut microbiota. Nutrients. V. 13, No. 1 (2020): p. 7. DOI: 10.3390/nu13010007.

Milani C. et al. The first microbial colonizers of the human gut: composition, activities, and health impli-cations of the infant gut microbiota. Microbiology and molecular biology reviews. V. 81, No. 4 (2017): pp. 10-128. DOI: 10.1128/MMBR.00036-17.

Miquel S. et al. Faecalibacterium prausnitzii and human intestinal health. Current opinion in microbiol-ogy. V. 16, No. 3 (2013): pp. 255-261. DOI: 10.1016/j.mib.2013.06.003.

Mitsou E.K. et al. Adherence to the Mediterranean diet is associated with the gut microbiota pattern and gastrointestinal characteristics in an adult population. British Journal of Nutrition. V. 117, No. 12 (2017): pp. 1645-1655. DOI: 10.1017/S0007114517001593

Moon J. et al. Faecalibacterium prausnitzii alleviates inflammatory arthritis and regulates IL-17 produc-tion, short chain fatty acids, and the intestinal microbial flora in experimental mouse model for rheumatoid ar-thritis. Arthritis Research & Therapy. V. 25, No. 1 (2023): p. 130. DOI: 10.1186/s13075-023-03118-3.

Neal E.G. et al. A randomized trial of classical and medium‐chain triglyceride ketogenic diets in the treatment of childhood epilepsy. Epilepsia. V. 50, No. 5 (2009): pp. 1109-1117. DOI: 10.1111/j.1528-1167.2008.01870.x.

Nilsson N.E. et al. Identification of a free fatty acid receptor, FFA2R, expressed on leukocytes and acti-vated by short-chain fatty acids. Biochemical and biophysical research communications. V. 303, No. 4 (2003): pp. 1047-1052. DOI: 10.1016/s0006-291x(03)00488-1.

Olson C.A. et al. The gut microbiota mediates the anti-seizure effects of the ketogenic diet. Cell. V. 173, No. 7 (2018): pp. 1728-1741.e13. DOI: 10.1016/j.cell.2018.04.027.

Otálora-Otálora B.A. et al. Host Transcriptional Regulatory Genes and Microbiome Networks Crosstalk through Immune Receptors Establishing Normal and Tumor Multiomics Metafirm of the Oral-Gut-Lung Axis. International Journal of Molecular Sciences. V. 24, No. 23 (2023): p. 16638. DOI: 10.3390/ijms242316638.

Paoli A. et al. Ketogenic diet and microbiota: friends or enemies? Genes. V. 10, No. 7 (2019): p. 534. DOI: 10.3390/genes10070534.

Piche T. et al. Mast cells and cellularity of the colonic mucosa correlated with fatigue and depression in irritable bowel syndrome. Gut. V. 57, No. 4 (2008): pp. 468-473. DOI: 10.1136/gut.2007.127068.

Rodrigues R.R. et al. Transkingdom interactions between Lactobacilli and hepatic mitochondria attenu-ate western diet-induced diabetes. Nat. Commun. V. 12 (2021): p. 101. DOI: 10.1038/s41467-020-20313-x.

Routy B. et al. Gut microbiome influences efficacy of PD-1-based immunotherapy against epithelial tu-mors. Science. V. 359, No. 6371 (2018): pp. 91-97. DOI: 10.1126/science.aan3706.

Säemann M.D. et al. Anti‐inflammatory effects of sodium butyrate on human monocytes: potent inhibi-tion of IL‐12 and up‐regulation of IL‐10 production. The FASEB Journal. V. 14, No. 15 (2000): pp. 2380-2382. DOI: 10.1096/fj.00-0359fje.

Sakkas H. et al. Nutritional status and the influence of the vegan diet on the gut microbiota and human health. Medicina. V. 56, No. 2 (2020): p. 88. DOI: 10.3390/medicina56020088.

Sanz Y. Effects of a gluten-free diet on gut microbiota and immune function in healthy adult humans. Gut Microbes. V. 1, No. 3 (2010): pp. 135-137. DOI: 10.4161/gmic.1.3.11868.

Shen Z. et al. Insights into Roseburia intestinalis which alleviates experimental colitis pathology by induc-ing anti‐inflammatory responses. Journal of gastroenterology and hepatology. V. 33, No. 10 (2018): pp. 1751-1760. DOI: 10.1111/jgh.14144.

Shi N. et al. Interaction between the gut microbiome and mucosal immune system. Military Medical Re-search. V. 4 (2017): pp. 1-7. DOI: 10.1186/s40779-017-0122-9.

Shin N.R. et al. An increase in the Akkermansia spp. population induced by metformin treatment im-proves glucose homeostasis in diet-induced obese mice. Gut. V. 63, No. 5 (2014): pp. 727-735. DOI: 10.1136/gutjnl-2012-303839.

Singh R.K. et al. Influence of diet on the gut microbiome and implications for human health. Journal of translational medicine. V. 15, No. 1 (2017): pp. 1-17. DOI: 10.1186/s12967-017-1175-y.

Smith P.M. et al. The microbial metabolites, short-chain fatty acids, regulate colonic Treg cell homeosta-sis. Science. V. 341, No. 6145 (2013): pp. 569-573. DOI: 10.1126/science.1241165.

Sokol H. et al. Faecalibacterium prausnitzii is an anti-inflammatory commensal bacterium identified by gut microbiota analysis of Crohn disease patients. Proceedings of the National Academy of Sciences. V. 105, No. 43 (2008): pp. 16731-16736. DOI: 10.1073/pnas.0804812105.

Staudacher H.M., Whelan K. The low FODMAP diet: recent advances in understanding its mechanisms and efficacy in IBS. Gut. V. 66, No. 8 (2017): pp. 1517-1527. DOI: 10.1136/gutjnl-2017-313750.

Tamanai-Shacoori Z. et al. Roseburia spp.: a marker of health? Future microbiology. 2017. V. 12, No. 2 (2017): pp. 157-170. DOI: 10.2217/fmb-2016-0130.

Tedelind S. et al. Anti-inflammatory properties of the short-chain fatty acids acetate and propionate: a study with relevance to inflammatory bowel disease. World journal of gastroenterology: WJG. V. 13, No. 20 (2007): p. 2826. DOI: 10.3748/wjg.v13.i20.2826.

Thananimit S., Pahumunto N., Teanpaisan R. Characterization of short chain fatty acids produced by selected potential probiotic Lactobacillus strains. Biomolecules. V. 12, No. 12 (2022): p. 1829. DOI: 10.3390/biom12121829.

Tomova A. et al. The effects of vegetarian and vegan diets on gut microbiota. Frontiers in nutrition. V. 6 (2019): p. 47. DOI: 10.3389/fnut.2019.00047.

Vinolo M.A. et al. SCFAs induce mouse neutrophil chemotaxis through the GPR43 receptor. PloS one. V. 6, No. 6 (2011): e21205. DOI: 10.1371/journal.pone.0021205.

Vinolo M.A. et al. Suppressive effect of short-chain fatty acids on production of proinflammatory medi-ators by neutrophils. The Journal of nutritional biochemistry. V. 22, No. 9 (2011): pp. 849-855. DOI: 10.1016/j.jnutbio.2010.07.009.

Vinolo M.A. et al. Regulation of inflammation by short chain fatty acids. Nutrients. V. 3, No. 10 (2011): pp. 858-876. DOI: 10.3390/nu3100858.

Walker C.R. et al. Intestinal intraepithelial lymphocyte-enterocyte crosstalk regulates production of bac-tericidal angiogenin 4 by Paneth cells upon microbial challenge. PLoS One. V. 8, No. 12 (2013): e84553. DOI: 10.1371/journal.pone.0084553.

Wrzosek L. et al. Bacteroides thetaiotaomicron and Faecalibacterium prausnitzii influence the produc-tion of mucus glycans and the development of goblet cells in the colonic epithelium of a gnotobiotic model ro-dent. BMC biology. V. 11, No. 61 (2013): pp. 1-13. DOI: 10.1186/1741-7007-11-61.

Xie G. et al. Ketogenic diet poses a significant effect on imbalanced gut microbiota in infants with refrac-tory epilepsy. World Journal of Gastroenterology. V. 23, No. 33 (2017): pp. 6164-6171. DOI: 10.3748/wjg.v23.i33.6164.

Yan H. et al. Gut microbiome alterations in patients with visceral obesity based on quantitative comput-ed tomography. Frontiers in Cellular and Infection Microbiology. V. 11 (2022): 823262. DOI: 10.3389/fcimb.2021.823262

Zafar H., Saier Jr M. H. Gut Bacteroides species in health and disease. Gut microbes. V. 13, No. 1 (2021): 1848158. DOI: 10.1080/19490976.2020.1848158.

, Zhai R. et al. Strain-specific anti-inflammatory properties of two Akkermansia muciniphila strains on chronic colitis in mice. Frontiers in cellular and infection microbiology. V. 9 (2019): p. 239. DOI: 10.3389/fcimb.2019.00239.

, Zhu C. et al. Roseburia intestinalis inhibits interleukin‑17 excretion and promotes regulatory T cells dif-ferentiation in colitis. Molecular medicine reports. V. 17, No. 6 (2018): pp. 7567-7574. DOI: 10.3892/mmr.2018.8833.

Most read articles by the same author(s)