The human gut microbiome: scientific paradigm shifts and clinical practice today and tomorrow
Keywords:
intestinal microbiome, core microbiome, enterotypes of microbiomes, directed microbiome restoration, fecal transplantation, synbiotics
Abstract
The study of the human microbiome, which began 15 years ago and is actively ongoing at the present time, has largely resulted in reconsideration of our views on the underlying mechanisms of interaction between the human body and the microorganisms inhabiting it. The picture that emerged has turned out to be much more complex than expected, especially for the gut microbiome. At present, the scientific concepts of what constitutes the gut microbiome are actively developing. They are based, of course,
on a reductionist approach. Thus, the theory of «a core microbiome» and the associated concept of «a healthy microbiome» have been proposed. An even more simplified approach to solving the problem of diversity and variability of intestinal microbiomes is the theory of «enterotypes.» It presupposes the existence of preferred (stable) variants of microbiomes structurally organized around certain groups of microorganisms. If anaerobic gram-negative rods are structure-forming, then such microbiomes are
characterized by low species diversity, dominance of a small group of microorganisms, and low stress resistance. These types of microbiomes are found in patients with various pathologies, including extraintestinally localized. Therefore, it is assumed that stratification of microbiomes based on enterotypes is convenient from the practical point of view. At present, the scientific concept of microbiomes has little input into medical practice. However, the already existing experience of using pre- and symbiotics, bacteriophages and fecal transplantation indicates the real possibility of changing microbiomes for the prevention and treatment of various human diseases.
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References
1. Li J., Jia H., Cai X., Zhong H., Feng Q., Sunagawa S., et al.; MetaHIT Consortium. An integrated catalog of reference genes in the human gut microbiome. Nat. Biotechnol. 2014;32(8):834-841. https://doi.org/10.1038/nbt.2942
2. Sender R., Fuchs S., Milo R. Are We Really Vastly Outnumbered? Revisiting the Ratio of Bacterial to Host Cells in Humans. Cell. 2016;164(3):337-340. https://doi.org/10.1016/j.cell.2016.01.013
3. Kedia S., Ahuja V. Human gut microbiome: A primer for the clinician. JGH Open. 2023;7(5):337-350. https://doi.org/10.1002/jgh3.12902 eCollection 2023 May.
4. Chang Y., Hou F., Pan Z., Huang Z., Han N., Bin L., et al. Optimization of Culturomics Strategy in Human Fecal Samples. Front Microbiol. 2019;10:2891. https://doi.org/10.3389/fmicb.2019.02891 eCollection 2019.
5. Marchesi J.R., Adams D.H., Fava F., Hermes G.D., Hirschfield G.M., Hold G., et al. The gut microbiota and host health: a new clinical frontier. Gut. 2016;65(2):330-339. https://doi.org/10.1136/gutjnl-2015-309990
6. Nielsen H.B., Almeida M., Juncker A.S., Rasmussen S., Li J., Sunagawa S., et al. Identification and assembly of genomes and genetic elements in complex metagenomic samples without using reference genomes. Nat. Biotechnol. 2014;32(8):822–828. https://doi.org/10.1038/nbt.2939
7. He Y., Wu W., Zheng H.M., Li P., McDonald D., Sheng H.F., et al. Regional variation limits applications of healthy gut microbiome reference ranges and disease models. Nat. Med. 2018;24(10):1532-1535. https://doi.org/10.1038/s41591-018-0164-x
8. Li W., O'Neill K.R., Haft D.H., DiCuccio M., Chetvernin V., Badretdin A., et al. RefSeq: expanding the Prokaryotic Genome Annotation Pipeline reach with protein family model curation. Nucleic. Acids. Res. 2021;49(D1):D1020-D1028. https://doi.org/10.1093/nar/gkaa1105
9. Milanese A., Mende D.R., Paoli L., Salazar G., Ruscheweyh H.J., Cuenca M., et al. Microbial abundance, activity and population genomic profiling with mOTUs2. Nat. Commun. 2019;10(1):1014. https://doi.org/10.1038/s41467-019-08844-4
10. Meziti A., Rodriguez-R L.M., Hatt J.K., Peña-Gonzalez A., Levy K., Konstantinidis K.T. The Reliability of Metagenome-Assembled Genomes (MAGs) in Representing Natural Populations: Insights from Comparing MAGs against Isolate Genomes Derived from the Same Fecal Sample. Appl. Environ. Microbiol. 2021;87(6):e02593-20. https://doi.org/10.1128/AEM.02593-20
11. Allaband C., McDonald D., Vázquez-Baeza Y., Minich J.J., Tripathi A., Brenner D.A., et al. Microbiome 101: Studying, Analyzing, and Interpreting Gut Microbiome Data for Clinicians. Clin. Gastroenterol. Hepatol. 2019;17(2):218-230. https://doi.org/10.1016/j.cgh.2018.09.017
12. Watson A.R., Füssel J., Veseli I., DeLongchamp J.Z., Silva M., Trigodet F., et al. Metabolic independence drives gut microbial colonization and resilience in health and disease. Genome Biol. 2023;24(1):78. https://doi.org/10.1186/s13059-023-02924-x
13. Wexler A.G., Goodman A.L. An insider’s perspective: Bacteroides as a window into the microbiome. Nat. Microbiol. 2017;2:17026. https://doi.org/10.1038/nmicrobiol.2017.26
14. Eisenstein M. The hunt for a healthy microbiome. Nature. 2020;577(7792):S6–S8. https://doi.org/10.1038/d41586-020-00193-3
15. Lloyd-Price J, Mahurkar A, Rahnavard G, Crabtree J, Orvis J, Hall AB, et al. Strains, functions and dynamics in the expanded Human Microbiome Project. Nature. 2017;550(7674):61–66. https://doi.org/10.1038/nature23889
16. Wu G., Zhao N., Zhang C., Lam Y.Y., Zhao L. Guild-based analysis for understanding gut microbiome in human health and diseases. Genome Med. 2021;13(1):22. https://doi.org/10.1186/s13073-021-00840-y
17. McKeown N.M., Fahey G.C. Jr, Slavin J., van der Kamp J.W. Fibre intake for optimal health: how can healthcare professionals support people to reach dietary recommendations? BMJ. 2022;378:e054370. https://doi.org/10.1136/bmj-2020-054370
18. Human Microbiome Project Consortium. Structure, function and diversity of the healthy human microbiome. Nature. 2012;486(7402):207–214. https://doi.org/10.1038/nature11234
19. Whon T.W., Shin N.R., Kim J.Y., Roh S.W. Omics in gut microbiome analysis. J. Microbiol. 2021;59(3):292-297. https://doi.org/10.1007/s12275-021-1004-0
20. Tian L., Wang X.W., Wu A.K., Fan Y., Friedman J., Dahlin A., et al. Deciphering functional redundancy in the human microbiome. Nat. Commun. 2020;11(1):6217. https://doi.org/10.1038/s41467-020-19940-1
21. Costea P.I., Hildebrand F., Arumugam M., Bäckhed F., Blaser M.J., Bushman F.D., et al. Enterotypes in the landscape of gut microbial community composition. Nat. Microbiol. 2018;3(1):8-16. https://doi.org/10.1038/s41564-017-0072-8
22. Arumugam M., Raes J., Pelletier E., Le Paslier D., Yamada T., Mende D.R., et al. Enterotypes of the human gut microbiome. Nature. 2011;473(7346):174-180. https://doi.org/10.1038/nature09944
23. Vieira-Silva S., Falony G., Darzi Y., Lima-Mendez G., Garcia Yunta R., Okuda S., et al. Species–function relationships shape ecological properties of the human gut microbiome. Nat. Microbiol. 2016;1(8):16088. https://doi.org/10.1038/nmicrobiol.2016.88
24. Pereira F.C., Berry D. Microbial nutrient niches in the gut. Environ Microbiol. 2017;19(4):1366–1378. https://doi.org/10.1111/1462-2920.13659
25. Couch C.E., Stagaman K., Spaan R.S., Combrink H.J., Sharpton T.J., Beechler B.R., et al. Diet and gut microbiome enterotype are associated at the population level in African buffalo. Nat. Commun. 2021;12(1):2267. https://doi.org/10.1038/s41467-021-22510-8
26. Chevalier C., Stojanović O., Colin D.J., Suarez-Zamorano N., Tarallo V., Veyrat-Durebex C., et al. Gut microbiota orchestrates energy homeostasis during cold. Cell. 2015;163(6):1360–1374. https://doi.org/10.1016/j.cell.2015.11.004
27. de la Cuesta-Zuluaga J., Mueller N.T., Corrales-Agudelo V., Velásquez-Mejía E.P., Carmona J.A., Abad J.M., et al. Metformin Is Associated with Higher Relative Abundance of Mucin-Degrading Akkermansia muciniphila and Several Short-Chain Fatty Acid-Producing Microbiota in the Gut. Diabetes Care. 2017;40(1):54-62. https://doi.org/10.2337/dc16-1324
28. Chung M., Zhao N., Meier R., Koestler D. C., Wu G., de Castillo E., et al. Comparisons of oral, intestinal, and pancreatic bacterial microbiomes in patients with pancreatic cancer and other gastrointestinal diseases. J. Oral Microbiol. 2021;13(1):1887680. https://doi.org/10.1080/20002297.2021.1887680
29. Khorsand B., Asadzadeh Aghdaei H., Nazemalhosseini-Mojarad E., Nadalian B., Nadalian B., Houri H. Overrepresentation of Enterobacteriaceae and Escherichia coli is the major gut microbiome signature in Crohn's disease and ulcerative colitis; a comprehensive metagenomic analysis of IBDMDB datasets. Front. Cell. Infect. Microbiol. 2022;12:1015890. https://doi.org/10.3389/fcimb.2022.1015890 eCollection 2022.
30. Magne F., Gotteland M., Gauthier L., Zazueta A., Pesoa S., Navarrete P., et al. The Firmicutes/Bacteroidetes Ratio: A Relevant Marker of Gut Dysbiosis in Obese Patients? Nutrients. 2020;12(5):1474. https://doi.org/10.3390/nu12051474
2. Sender R., Fuchs S., Milo R. Are We Really Vastly Outnumbered? Revisiting the Ratio of Bacterial to Host Cells in Humans. Cell. 2016;164(3):337-340. https://doi.org/10.1016/j.cell.2016.01.013
3. Kedia S., Ahuja V. Human gut microbiome: A primer for the clinician. JGH Open. 2023;7(5):337-350. https://doi.org/10.1002/jgh3.12902 eCollection 2023 May.
4. Chang Y., Hou F., Pan Z., Huang Z., Han N., Bin L., et al. Optimization of Culturomics Strategy in Human Fecal Samples. Front Microbiol. 2019;10:2891. https://doi.org/10.3389/fmicb.2019.02891 eCollection 2019.
5. Marchesi J.R., Adams D.H., Fava F., Hermes G.D., Hirschfield G.M., Hold G., et al. The gut microbiota and host health: a new clinical frontier. Gut. 2016;65(2):330-339. https://doi.org/10.1136/gutjnl-2015-309990
6. Nielsen H.B., Almeida M., Juncker A.S., Rasmussen S., Li J., Sunagawa S., et al. Identification and assembly of genomes and genetic elements in complex metagenomic samples without using reference genomes. Nat. Biotechnol. 2014;32(8):822–828. https://doi.org/10.1038/nbt.2939
7. He Y., Wu W., Zheng H.M., Li P., McDonald D., Sheng H.F., et al. Regional variation limits applications of healthy gut microbiome reference ranges and disease models. Nat. Med. 2018;24(10):1532-1535. https://doi.org/10.1038/s41591-018-0164-x
8. Li W., O'Neill K.R., Haft D.H., DiCuccio M., Chetvernin V., Badretdin A., et al. RefSeq: expanding the Prokaryotic Genome Annotation Pipeline reach with protein family model curation. Nucleic. Acids. Res. 2021;49(D1):D1020-D1028. https://doi.org/10.1093/nar/gkaa1105
9. Milanese A., Mende D.R., Paoli L., Salazar G., Ruscheweyh H.J., Cuenca M., et al. Microbial abundance, activity and population genomic profiling with mOTUs2. Nat. Commun. 2019;10(1):1014. https://doi.org/10.1038/s41467-019-08844-4
10. Meziti A., Rodriguez-R L.M., Hatt J.K., Peña-Gonzalez A., Levy K., Konstantinidis K.T. The Reliability of Metagenome-Assembled Genomes (MAGs) in Representing Natural Populations: Insights from Comparing MAGs against Isolate Genomes Derived from the Same Fecal Sample. Appl. Environ. Microbiol. 2021;87(6):e02593-20. https://doi.org/10.1128/AEM.02593-20
11. Allaband C., McDonald D., Vázquez-Baeza Y., Minich J.J., Tripathi A., Brenner D.A., et al. Microbiome 101: Studying, Analyzing, and Interpreting Gut Microbiome Data for Clinicians. Clin. Gastroenterol. Hepatol. 2019;17(2):218-230. https://doi.org/10.1016/j.cgh.2018.09.017
12. Watson A.R., Füssel J., Veseli I., DeLongchamp J.Z., Silva M., Trigodet F., et al. Metabolic independence drives gut microbial colonization and resilience in health and disease. Genome Biol. 2023;24(1):78. https://doi.org/10.1186/s13059-023-02924-x
13. Wexler A.G., Goodman A.L. An insider’s perspective: Bacteroides as a window into the microbiome. Nat. Microbiol. 2017;2:17026. https://doi.org/10.1038/nmicrobiol.2017.26
14. Eisenstein M. The hunt for a healthy microbiome. Nature. 2020;577(7792):S6–S8. https://doi.org/10.1038/d41586-020-00193-3
15. Lloyd-Price J, Mahurkar A, Rahnavard G, Crabtree J, Orvis J, Hall AB, et al. Strains, functions and dynamics in the expanded Human Microbiome Project. Nature. 2017;550(7674):61–66. https://doi.org/10.1038/nature23889
16. Wu G., Zhao N., Zhang C., Lam Y.Y., Zhao L. Guild-based analysis for understanding gut microbiome in human health and diseases. Genome Med. 2021;13(1):22. https://doi.org/10.1186/s13073-021-00840-y
17. McKeown N.M., Fahey G.C. Jr, Slavin J., van der Kamp J.W. Fibre intake for optimal health: how can healthcare professionals support people to reach dietary recommendations? BMJ. 2022;378:e054370. https://doi.org/10.1136/bmj-2020-054370
18. Human Microbiome Project Consortium. Structure, function and diversity of the healthy human microbiome. Nature. 2012;486(7402):207–214. https://doi.org/10.1038/nature11234
19. Whon T.W., Shin N.R., Kim J.Y., Roh S.W. Omics in gut microbiome analysis. J. Microbiol. 2021;59(3):292-297. https://doi.org/10.1007/s12275-021-1004-0
20. Tian L., Wang X.W., Wu A.K., Fan Y., Friedman J., Dahlin A., et al. Deciphering functional redundancy in the human microbiome. Nat. Commun. 2020;11(1):6217. https://doi.org/10.1038/s41467-020-19940-1
21. Costea P.I., Hildebrand F., Arumugam M., Bäckhed F., Blaser M.J., Bushman F.D., et al. Enterotypes in the landscape of gut microbial community composition. Nat. Microbiol. 2018;3(1):8-16. https://doi.org/10.1038/s41564-017-0072-8
22. Arumugam M., Raes J., Pelletier E., Le Paslier D., Yamada T., Mende D.R., et al. Enterotypes of the human gut microbiome. Nature. 2011;473(7346):174-180. https://doi.org/10.1038/nature09944
23. Vieira-Silva S., Falony G., Darzi Y., Lima-Mendez G., Garcia Yunta R., Okuda S., et al. Species–function relationships shape ecological properties of the human gut microbiome. Nat. Microbiol. 2016;1(8):16088. https://doi.org/10.1038/nmicrobiol.2016.88
24. Pereira F.C., Berry D. Microbial nutrient niches in the gut. Environ Microbiol. 2017;19(4):1366–1378. https://doi.org/10.1111/1462-2920.13659
25. Couch C.E., Stagaman K., Spaan R.S., Combrink H.J., Sharpton T.J., Beechler B.R., et al. Diet and gut microbiome enterotype are associated at the population level in African buffalo. Nat. Commun. 2021;12(1):2267. https://doi.org/10.1038/s41467-021-22510-8
26. Chevalier C., Stojanović O., Colin D.J., Suarez-Zamorano N., Tarallo V., Veyrat-Durebex C., et al. Gut microbiota orchestrates energy homeostasis during cold. Cell. 2015;163(6):1360–1374. https://doi.org/10.1016/j.cell.2015.11.004
27. de la Cuesta-Zuluaga J., Mueller N.T., Corrales-Agudelo V., Velásquez-Mejía E.P., Carmona J.A., Abad J.M., et al. Metformin Is Associated with Higher Relative Abundance of Mucin-Degrading Akkermansia muciniphila and Several Short-Chain Fatty Acid-Producing Microbiota in the Gut. Diabetes Care. 2017;40(1):54-62. https://doi.org/10.2337/dc16-1324
28. Chung M., Zhao N., Meier R., Koestler D. C., Wu G., de Castillo E., et al. Comparisons of oral, intestinal, and pancreatic bacterial microbiomes in patients with pancreatic cancer and other gastrointestinal diseases. J. Oral Microbiol. 2021;13(1):1887680. https://doi.org/10.1080/20002297.2021.1887680
29. Khorsand B., Asadzadeh Aghdaei H., Nazemalhosseini-Mojarad E., Nadalian B., Nadalian B., Houri H. Overrepresentation of Enterobacteriaceae and Escherichia coli is the major gut microbiome signature in Crohn's disease and ulcerative colitis; a comprehensive metagenomic analysis of IBDMDB datasets. Front. Cell. Infect. Microbiol. 2022;12:1015890. https://doi.org/10.3389/fcimb.2022.1015890 eCollection 2022.
30. Magne F., Gotteland M., Gauthier L., Zazueta A., Pesoa S., Navarrete P., et al. The Firmicutes/Bacteroidetes Ratio: A Relevant Marker of Gut Dysbiosis in Obese Patients? Nutrients. 2020;12(5):1474. https://doi.org/10.3390/nu12051474
Published
2024-06-22
How to Cite
Evdokimova N. V., Chernenkaya T. V. The human gut microbiome: scientific paradigm shifts and clinical practice today and tomorrow // Patologicheskaya Fiziologiya i Eksperimental’naya Terapiya (Pathological physiology and experimental therapy). 2024. VOL. 68. № 2. PP. 76–86.
Issue
Section
Reviews
