Effects from diet-induced gut microbiota dysbiosis and obesity can be ameliorated by fecal microbiota transplantation: A multiomics approach
Autoři:
Maria Guirro aff001; Andrea Costa aff002; Andreu Gual-Grau aff001; Pol Herrero aff002; Helena Torrell aff002; Núria Canela aff002; Lluis Arola aff001
Působiště autorů:
Universitat Rovira i Virgili, Biochemistry and Biotechnology Department, Nutrigenomics Research Group, Tarragona, Spain
aff001; Eurecat, Centre Tecnològic de Catalunya, Centre for Omic Sciences (COS), Joint Unit Universitat Rovira i Virgili-EURECAT, Unique Scientific and Technical Infrastructures (ICTS), Reus, Spain
aff002; Eurecat, Centre Tecnològic de Catalunya, Biotechnological Area, Reus, Spain
aff003
Vyšlo v časopise:
PLoS ONE 14(9)
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pone.0218143
Souhrn
Obesity and its comorbidities are currently considered an epidemic, and the involved pathophysiology is well studied. Hypercaloric diets are tightly related to the obesity etiology and also cause alterations in gut microbiota functionality. Diet and antibiotics are known to play crucial roles in changes in the microbiota ecosystem and the disruption of its balance; therefore, the manipulation of gut microbiota may represent an accurate strategy to understand its relationship with obesity caused by diet. Fecal microbiota transplantation, during which fecal microbiota from a healthy donor is transplanted to an obese subject, has aroused interest as an effective approach for the treatment of obesity. To determine its success, a multiomics approach was used that combined metagenomics and metaproteomics to study microbiota composition and function. To do this, a study was performed in rats that evaluated the effect of a hypercaloric diet on the gut microbiota, and this was combined with antibiotic treatment to deplete the microbiota before fecal microbiota transplantation to verify its effects on gut microbiota-host homeostasis. Our results showed that a high-fat diet induces changes in microbiota biodiversity and alters its function in the host. Moreover, we found that antibiotics depleted the microbiota enough to reduce its bacterial content. Finally, we assessed the use of fecal microbiota transplantation as a complementary obesity therapy, and we found that it reversed the effects of antibiotics and reestablished the microbiota balance, which restored normal functioning and alleviated microbiota disruption. This new approach could be implemented to support the dietary and healthy habits recommended as a first option to maintain the homeostasis of the microbiota.
Klíčová slova:
Diet – Antibiotics – Obesity – Microbiome – Metagenomics – Gut bacteria – Clostridium – Metabolic pathways
Zdroje
1. Shen J, Obin MS, Zhao L. The gut microbiota, obesity and insulin resistance. Mol Aspects Med. Elsevier Ltd; 2013;34: 39–58. doi: 10.1016/j.mam.2012.11.001 23159341
2. Heymsfield SB, Wadden TA. Mechanisms, Pathophysiology, and Management of Obesity. N Engl J Med. 2017;376: 254–266. doi: 10.1056/NEJMra1514009 28099824
3. Grasa L, Abecia L, Forcén R, Castro M, de Jalón JAG, Latorre E, et al. Antibiotic-Induced Depletion of Murine Microbiota Induces Mild Inflammation and Changes in Toll-Like Receptor Patterns and Intestinal Motility. Microb Ecol. 2015;70: 835–848. doi: 10.1007/s00248-015-0613-8 25896428
4. Cani PD, Delzenne NM. The gut microbiome as therapeutic target. Pharmacol Ther. Elsevier Inc.; 2011;130: 202–212. doi: 10.1016/j.pharmthera.2011.01.012 21295072
5. Ottman N, Smidt H, de Vos WM, Belzer C. The function of our microbiota: who is out there and what do they do? Front Cell Infect Microbiol. 2012;2: 104. doi: 10.3389/fcimb.2012.00104 22919693
6. Buettner R, Schölmerich J, Bollheimer LC. High-fat diets: Modeling the metabolic disorders of human obesity in rodents. Obesity. 2007. pp. 798–808. doi: 10.1038/oby.2007.608 17426312
7. Nilsson C, Raun K, Yan F, Larsen MO, Tang-Christensen M. Laboratory animals as surrogate models of human obesity. Acta Pharmacol Sin. 2012;33: 173–181. doi: 10.1038/aps.2011.203 22301857
8. Zhao L, Zhang Q, Ma W, Tian F, Shen H, Zhou M. A combination of quercetin and resveratrol reduces obesity in high-fat diet-fed rats by modulation of gut microbiota. Food Funct. England; 2017;8: 4644–4656. doi: 10.1039/c7fo01383c 29152632
9. Boi SK, Buchta CM, Pearson NA, Francis MB, Meyerholz DK, Grobe JL, et al. Obesity alters immune and metabolic profiles: New insight from obese-resistant mice on high-fat diet. Obesity (Silver Spring). United States; 2016;24: 2140–2149. doi: 10.1002/oby.21620 27515998
10. Ha M, Sabherwal M, Duncan E, Stevens S, Stockwell P, McConnell M, et al. In-Depth Characterization of Sheep (Ovis aries) Milk Whey Proteome and Comparison with Cow (Bos taurus). PLoS One. United States; 2015;10: e0139774. doi: 10.1371/journal.pone.0139774 26447763
11. Janssen AWF, Kersten S. The role of the gut microbiota in metabolic health. FASEB J. 2015;9: 577–589. doi: 10.1096/fj.14-269514
12. Lee P, Yacyshyn BR, Yacyshyn MB. Gut microbiota and obesity: An opportunity to alter obesity through faecal microbiota transplant (FMT). Diabetes, Obes Metab. 2018; doi: 10.1111/dom.13561 30328245
13. Lai ZL, Tseng CH, Ho HJ, Cheung CKY, Lin JY, Chen YJ, et al. Fecal microbiota transplantation confers beneficial metabolic effects of diet and exercise on diet-induced obese mice. Sci Rep. 2018;8: 1–11. doi: 10.1038/s41598-017-17765-5
14. Sun W, Guo Y, Zhang S, Chen Z, Wu K, Liu Q, et al. Fecal Microbiota Transplantation Can Alleviate Gastrointestinal Transit in Rats with High-Fat Diet-Induced Obesity via Regulation of Serotonin Biosynthesis. Biomed Res Int. Hindawi; 2018;2018. doi: 10.1155/2018/8308671 30370307
15. Schuijt TJ, Lankelma JM, Scicluna BP, De Sousa E Melo F, Roelofs JJTH, JD De Boer, et al. The gut microbiota plays a protective role in the host defence against pneumococcal pneumonia. Gut. 2016;65: 575–583. doi: 10.1136/gutjnl-2015-309728 26511795
16. Le Bastard Q, Ward T, Sidiropoulos D, Hillmann BM, Chun CL, Sadowsky MJ, et al. Fecal microbiota transplantation reverses antibiotic and chemotherapy-induced gut dysbiosis in mice. Sci Rep. Springer US; 2018;8: 1–11. doi: 10.1038/s41598-017-17765-5
17. Wang S, Huang M, You X, Zhao J, Chen L, Wang L, et al. Gut microbiota mediates the anti-obesity effect of calorie restriction in mice. Sci Rep. Springer US; 2018;8: 2–15. doi: 10.1038/s41598-017-18521-5
18. Zhou D, Pan Q, Shen F, Cao HX, Ding WJ, Chen YW, et al. Total fecal microbiota transplantation alleviates high-fat diet-induced steatohepatitis in mice via beneficial regulation of gut microbiota. Sci Rep. Springer US; 2017;7: 1–11. doi: 10.1038/s41598-016-0028-x
19. Daniel H, Gholami AM, Berry D, Desmarchelier C, Hahne H, Loh G, et al. High-fat diet alters gut microbiota physiology in mice. ISME J. 2014;8: 295–308. doi: 10.1038/ismej.2013.155 24030595
20. del Bas JM, Guirro M, Boqué N, Cereto A, Ras R, Crescenti A, et al. Alterations in gut microbiota associated with a cafeteria diet and the physiological consequences in the host. Int J Obes. Macmillan Publishers Limited, part of Springer Nature; 2017; Available: http://dx.doi.org/10.1038/ijo.2017.284
21. Guirro M, Costa A, Gual-Grau A, Mayneris-Perxachs J, Torrell H, Herrero P, et al. Multi-omics approach to elucidate the gut microbiota activity: Metaproteomics and metagenomics connection. Electrophoresis. 2018;39: 1692–1701. doi: 10.1002/elps.201700476 29427518
22. Tanca A, Manghina V, Fraumene C, Palomba A, Abbondio M, Deligios M, et al. Metaproteogenomics reveals taxonomic and functional changes between cecal and fecal microbiota in mouse. Front Microbiol. 2017;8: 391. doi: 10.3389/fmicb.2017.00391 28352255
23. Bäckhed F, Ding H, Wang T, Hooper L V, Koh GY, Nagy A, et al. The gut microbiota as an environmental factor that regulates fat storage. Proc Natl Acad Sci U S A. 2004;101: 15718–23. doi: 10.1073/pnas.0407076101 15505215
24. Reikvam DH, Erofeev A, Sandvik A, Grcic V, Jahnsen FL, Gaustad P, et al. Depletion of murine intestinal microbiota: Effects on gut mucosa and epithelial gene expression. PLoS One. 2011;6: 1–13. doi: 10.1371/journal.pone.0017996 21445311
25. Hernández-Jarguín A, Díaz-Sánchez S, Villar M, de la Fuente J. Integrated metatranscriptomics and metaproteomics for the characterization of bacterial microbiota in unfed Ixodes ricinus. Ticks Tick Borne Dis. Elsevier; 2018;9: 1241–1251. doi: 10.1016/j.ttbdis.2018.04.020 29753651
26. Xiao M, Yang J, Feng Y, Zhu Y, Chai X, Wang Y. Metaproteomic strategies and applications for gut microbial research. Appl Microbiol Biotechnol. Applied Microbiology and Biotechnology; 2017;101: 3077–3088. doi: 10.1007/s00253-017-8215-7 28293710
27. Wei F, Wu Q, Hu Y, Huang G, Nie Y, Yan L. Conservation metagenomics: a new branch of conservation biology. Sci China Life Sci. China; 2018; doi: 10.1007/s11427-018-9423-3 30588567
28. Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, et al. QIIME allows analysis of high-throughput community sequencing data. Nat Methods. 2011;7: 335–336. doi: 10.1038/nmeth.f.303.QIIME
29. Guirro M, Herrero P, Costa A, Gual-Grau A, Ceretó-Massagué A, Hernández A, et al. Deciphering the functions of gut microbiota in an animal model of obesity using an optimized metaproteomics workflow. J Proteome Res. 2019;Submitted.
30. Lee S, Keirsey KI, Kirkland R, Grunewald ZI, Fischer JG, de La Serre CB. Blueberry Supplementation Influences the Gut Microbiota, Inflammation, and Insulin Resistance in High-Fat-Diet-Fed Rats. J Nutr. United States; 2018;148: 209–219. doi: 10.1093/jn/nxx027 29490092
31. Behr C, Kamp H, Fabian E, Krennrich G, Mellert W, Peter E, et al. Gut microbiome-related metabolic changes in plasma of antibiotic-treated rats. Arch Toxicol. Springer Berlin Heidelberg; 2017;91: 3439–3454. doi: 10.1007/s00204-017-1949-2 28337503
32. Tulstrup MVL, Christensen EG, Carvalho V, Linninge C, Ahrné S, Højberg O, et al. Antibiotic Treatment Affects Intestinal Permeability and Gut Microbial Composition in Wistar Rats Dependent on Antibiotic Class. PLoS One. 2015;10: 1–17. doi: 10.1371/journal.pone.0144854 26691591
33. Hoban AE, Moloney RD, Golubeva A V., McVey Neufeld KA, O’Sullivan O, Patterson E, et al. Behavioural and neurochemical consequences of chronic gut microbiota depletion during adulthood in the rat. Neuroscience. IBRO; 2016;339: 463–477. doi: 10.1016/j.neuroscience.2016.10.003 27742460
34. Lamendella R, Santo Domingo JW, Ghosh S, Martinson J, Oerther DB. Comparative fecal metagenomics unveils unique functional capacity of the swine gut. BMC Microbiol. BioMed Central Ltd; 2011;11: 103. doi: 10.1186/1471-2180-11-103 21575148
35. Villamil SI, Huerlimann R, Morianos C, Sarnyai Z, Maes GE. Adverse effect of early-life high-fat/high-carbohydrate (“Western”) diet on bacterial community in the distal bowel of mice. Nutr Res. Elsevier Inc.; 2018;50: 25–36. doi: 10.1016/j.nutres.2017.11.008 29540269
36. Zhang Y, Limaye PB, Renaud HJ, Klaassen CD. Effect of various antibiotics on modulation of intestinal microbiota and bile acid profile in mice. Toxicol Appl Pharmacol. Elsevier Inc.; 2014;277: 138–145. doi: 10.1016/j.taap.2014.03.009 24657338
37. Verdú EF, Bercik P, Verma-Gandhu M, Huang XX, Blennerhassett P, Jackson W, et al. Specific probiotic therapy attenuates antibiotic induced visceral hypersensitivity in mice. Gut. 2006;55: 182–190. doi: 10.1136/gut.2005.066100 16105890
38. Fröhlich EE, Farzi A, Mayerhofer R, Reichmann F, Jačan A, Wagner B, et al. Cognitive impairment by antibiotic-induced gut dysbiosis: Analysis of gut microbiota-brain communication. Brain Behav Immun. 2016;56: 140–155. doi: 10.1016/j.bbi.2016.02.020 26923630
39. Matsunaga N, Shimizu H, Fujimoto K, Watanabe K, Yamasaki T, Hatano N, et al. Expression of glyceraldehyde-3-phosphate dehydrogenase on the surface of Clostridium perfringens cells. Anaerobe. England; 2018;51: 124–130. doi: 10.1016/j.anaerobe.2018.05.001 29753109
40. Schreiber W, Durre P. The glyceraldehyde-3-phosphate dehydrogenase of Clostridium acetobutylicum: isolation and purification of the enzyme, and sequencing and localization of the gap gene within a cluster of other glycolytic genes. Microbiology. England; 1999;145 (Pt 8: 1839–1847. doi: 10.1099/13500872-145-8-1839 10463150
41. Oberbach A, Haange SB, Schlichting N, Heinrich M, Lehmann S, Till H, et al. Metabolic in Vivo Labeling Highlights Differences of Metabolically Active Microbes from the Mucosal Gastrointestinal Microbiome between High-Fat and Normal Chow Diet. J Proteome Res. 2017;16: 1593–1604. doi: 10.1021/acs.jproteome.6b00973 28252966
42. Heinritz SN, Weiss E, Eklund M, Aumiller T, Louis S, Rings A, et al. Intestinal microbiota and microbial metabolites are changed in a pig model fed a high-fat/low-fiber or a low-fat/high-fiber diet. PLoS One. 2016;11: 1–21. doi: 10.1371/journal.pone.0154329 27100182
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