Advertisement

Bariatric/Metabolic Surgery Induces Noticeable Changes of Microbiota and Their Secreting Extracellular Vesicle Composition in the Gut

  • Yeon-Ju Huh
  • Joo-Young Seo
  • Jieun Nam
  • Jinho Yang
  • Andrea McDowell
  • Yoon-Keun Kim
  • Joo-Ho LeeEmail author
Original Contributions
  • 127 Downloads

Abstract

Introduction

Microbial ecology is reported to be an important regulator of energy homeostasis and glucose metabolism. Microbes secrete extracellular vesicles (EVs) during their proliferation and death to communicate with other cells. To investigate the roles of gut microbiota in glucose metabolism, we analyzed serial changes of gut microbe and microbial EV composition before and after bariatric/metabolic surgery (BMS).

Methods

Twenty-eight Wistar rats were fed on high-fat diet (HFD) to induce obesity and diabetes. Five of them compared with 5 rats fed on regular chow diet (RCD). Among the remaining 23 rats, Roux-en-Y gastric bypass (RYGB) (n = 10), sleeve gastrectomy (SG) (n = 10), or sham operation (n = 3) was randomly performed. Gut microbiota and EVs from fecal samples were analyzed by 16S rDNA amplicon sequencing.

Results

The present study showed that microbial diversity was decreased in HFD-fed rats versus RCD-fed rats. In addition, BMS reversed glucose intolerance and microbial richness which were induced by HFD. In terms of microbiota and microbial EV composition, both RYGB and SG enhance the composition of phyla Proteobacteria, Verrucomicrobia, and their secreting EVs, but decrease phylum Firmicutes and its EVs. We tried to demonstrate specific genera showed a significant compositional difference in obesity/diabetes-induced rats compared with normal rats and then restored similarly toward normal rats’ level after BMS. At the genus level, Lactococcus, Ruminococcus, Dorea in Firmicutes(p), Psychrobacter in Proteobacteria(p), and Akkermansia in Verrucomicrobia(p) fit these conditions after BMS.

Conclusion

We suggest that these genera are the candidates contributing to obesity and diabetes improvement mechanism after BMS.

Keywords

Gut microbiota Extracellular vesicle Obesity Diabetes Bariatric/metabolic surgery 

Notes

Acknowledgements

This study was presented at the 22nd World Congress of international federation for the surgery of Obesity and Metabolic Disorders (IFSO 2017).

Funding

This research was supported by the Basic Science Research Program through the National Research Foundation of Korea (NRF) funded by the Ministry of Education (NRF-2016R1D1A1B03932360).

Compliance with Ethical Standards

The study protocol was reviewed and approved by the Institutional Animal Care and Use Committee of Ewha Womans University Mokdong Hospital (IACUC approval no. 15-0292).

Conflict of Interest

The authors declare that they have no conflict of interest.

Ethical Approval

The research followed all applicable institutional and/or national guidelines for the care and use of animals.

Supplementary material

11695_2019_3852_Fig8_ESM.png (1007 kb)
Fig. S1

(PNG 0.98 mb)

11695_2019_3852_MOESM1_ESM.tif (40.9 mb)
High resolution image (TIFF 40.9 mb)
11695_2019_3852_MOESM2_ESM.docx (15 kb)
Table S1 (DOCX 14.7 kb)

References

  1. 1.
    Obesity and overweight fact sheet 2018. Available at: http://www.who.int/news-room/fact-sheets/detail/obesity-and-overweight. Accessed July 31, 2018.
  2. 2.
    Schauer PR, Burguera B, Ikramuddin S, et al. Effect of laparoscopic Roux-en Y gastric bypass on type 2 diabetes mellitus. Ann Surg. 2003;238:5.Google Scholar
  3. 3.
    American Society for Metabolic and Bariatric Surgery. Type 2 diabetes and obesity: twin epidemics: American Society for Metabolic and Bariatric Surgery; 2013. https://asmbs.org/resources/weight-and-type-2-diabetes-after-bariatric-surgery-fact-sheet.
  4. 4.
    Karlsson FH, Fak F, Nookaew I, et al. Symptomatic atherosclerosis is associated with an altered gut metagenome. Nat Commun. 2012;3:1245.CrossRefGoogle Scholar
  5. 5.
    Scher JU, Sczesnak A, Longman RS, et al. Expansion of intestinal Prevotella copri correlates with enhanced susceptibility to arthritis. Elife. 2013;2:e01202.CrossRefGoogle Scholar
  6. 6.
    Qin N, Yang F, Li A, et al. Alterations of the human gut microbiome in liver cirrhosis. Nature. 2014;513:59–64.CrossRefGoogle Scholar
  7. 7.
    Zeller G, Tap J, Voigt AY, et al. Potential of fecal microbiota for early-stage detection of colorectal cancer. Mol Syst Biol. 2014;10:766.CrossRefGoogle Scholar
  8. 8.
    Ley RE, Backhed F, Turnbaugh P, et al. Obesity alters gut microbial ecology. Proc Natl Acad Sci U S A. 2005;102:11070–5.CrossRefGoogle Scholar
  9. 9.
    Turnbaugh PJ, Ley RE, Mahowald MA, et al. An obesity-associated gut microbiome with increased capacity for energy harvest. Nature. 2006;444:1027–31.CrossRefGoogle Scholar
  10. 10.
    Qin J, Li Y, Cai Z, et al. A metagenome-wide association study of gut microbiota in type 2 diabetes. Nature. 2012;490:55–60.CrossRefGoogle Scholar
  11. 11.
    Magouliotis DE, Tasiopoulou VS, Sioka E, et al. Impact of bariatric surgery on metabolic and gut microbiota profile: a systematic review and meta-analysis. Obes Surg. 2017;27:1345–57.CrossRefGoogle Scholar
  12. 12.
    Brown L, Wolf JM, Prados-Rosales R, et al. Through the wall: extracellular vesicles in gram-positive bacteria, mycobacteria and fungi. Nat Rev Microbiol. 2015;13:620–30.CrossRefGoogle Scholar
  13. 13.
    Yanez-Mo M, Siljander PR, Andreu Z, et al. Biological properties of extracellular vesicles and their physiological functions. J Extracellular Vesicles 2015;4:UNSP 27066.Google Scholar
  14. 14.
    Turnbaugh PJ, Backhed F, Fulton L, et al. Diet-induced obesity is linked to marked but reversible alterations in the mouse distal gut microbiome. Cell Host Microbe. 2008;3:213–23.CrossRefGoogle Scholar
  15. 15.
    Palleja A, Kashani A, Allin KH, et al. Roux-en-Y gastric bypass surgery of morbidly obese patients induces swift and persistent changes of the individual gut microbiota. Genome Med. 2016;8:67.CrossRefGoogle Scholar
  16. 16.
    Guo Y, Huang ZP, Liu CQ, et al. Modulation of the gut microbiome: a systematic review of the effect of bariatric surgery. Eur J Endocrinol. 2018;178:43–56.CrossRefGoogle Scholar
  17. 17.
    Kong LC, Tap J, Aron-Wisnewsky J, et al. Gut microbiota after gastric bypass in human obesity: increased richness and associations of bacterial genera with adipose tissue genes. Am J Clin Nutr. 2013;98:16–24.CrossRefGoogle Scholar
  18. 18.
    Ward EK, Schuster DP, Stowers KH, et al. The effect of PPI use on human gut microbiota and weight loss in patients undergoing laparoscopic Roux-en-Y gastric bypass. Obes Surg. 2014;24:1567–71.CrossRefGoogle Scholar
  19. 19.
    Guo Y, Liu CQ, Shan CX, et al. Gut microbiota after Roux-en-Y gastric bypass and sleeve gastrectomy in a diabetic rat model: increased diversity and associations of discriminant genera with metabolic changes. Diabetes Metab Res Rev. 2017;33  https://doi.org/10.1002/dmrr.2857.
  20. 20.
    Erejuwa OO, Sulaiman SA, Ab Wahab MS. Modulation of gut microbiota in the management of metabolic disorders: the prospects and challenges. Int J Mol Sci. 2014;15:4158–88.CrossRefGoogle Scholar
  21. 21.
    Choi Y, Kwon Y, Kim DK, et al. Gut microbe-derived extracellular vesicles induce insulin resistance, thereby impairing glucose metabolism in skeletal muscle. Sci Rep. 2015;5:15878.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  1. 1.LHK Bariatric and Metabolic ClinicSeoulRepublic of Korea
  2. 2.Department of SurgeryEwha Womans University College of MedicineSeoulRepublic of Korea
  3. 3.Department of MicrobiologyEwha Womans University College of MedicineSeoulRepublic of Korea
  4. 4.Institute of MD Healthcare Inc.SeoulRepublic of Korea

Personalised recommendations