Skip to main content
Top
Published in: Obesity Surgery 8/2019

01-08-2019 | Obesity | Original Contributions

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

Authors: Yeon-Ju Huh, Joo-Young Seo, Jieun Nam, Jinho Yang, Andrea McDowell, Yoon-Keun Kim, Joo-Ho Lee

Published in: Obesity Surgery | Issue 8/2019

Login to get access

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.
Appendix
Available only for authorised users
Literature
2.
go back to reference 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. 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.
4.
go back to reference Karlsson FH, Fak F, Nookaew I, et al. Symptomatic atherosclerosis is associated with an altered gut metagenome. Nat Commun. 2012;3:1245.CrossRef Karlsson FH, Fak F, Nookaew I, et al. Symptomatic atherosclerosis is associated with an altered gut metagenome. Nat Commun. 2012;3:1245.CrossRef
5.
go back to reference Scher JU, Sczesnak A, Longman RS, et al. Expansion of intestinal Prevotella copri correlates with enhanced susceptibility to arthritis. Elife. 2013;2:e01202.CrossRef Scher JU, Sczesnak A, Longman RS, et al. Expansion of intestinal Prevotella copri correlates with enhanced susceptibility to arthritis. Elife. 2013;2:e01202.CrossRef
6.
go back to reference Qin N, Yang F, Li A, et al. Alterations of the human gut microbiome in liver cirrhosis. Nature. 2014;513:59–64.CrossRef Qin N, Yang F, Li A, et al. Alterations of the human gut microbiome in liver cirrhosis. Nature. 2014;513:59–64.CrossRef
7.
go back to reference 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.CrossRef 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.CrossRef
8.
go back to reference Ley RE, Backhed F, Turnbaugh P, et al. Obesity alters gut microbial ecology. Proc Natl Acad Sci U S A. 2005;102:11070–5.CrossRef Ley RE, Backhed F, Turnbaugh P, et al. Obesity alters gut microbial ecology. Proc Natl Acad Sci U S A. 2005;102:11070–5.CrossRef
9.
go back to reference Turnbaugh PJ, Ley RE, Mahowald MA, et al. An obesity-associated gut microbiome with increased capacity for energy harvest. Nature. 2006;444:1027–31.CrossRef Turnbaugh PJ, Ley RE, Mahowald MA, et al. An obesity-associated gut microbiome with increased capacity for energy harvest. Nature. 2006;444:1027–31.CrossRef
10.
go back to reference 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.CrossRef 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.CrossRef
11.
go back to reference 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.CrossRef 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.CrossRef
12.
go back to reference 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.CrossRef 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.CrossRef
13.
go back to reference 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. 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.
14.
go back to reference 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.CrossRef 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.CrossRef
15.
go back to reference 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.CrossRef 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.CrossRef
16.
go back to reference 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.CrossRef 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.CrossRef
17.
go back to reference 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.CrossRef 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.CrossRef
18.
go back to reference 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.CrossRef 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.CrossRef
19.
20.
go back to reference 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.CrossRef 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.CrossRef
21.
go back to reference 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.CrossRef 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.CrossRef
Metadata
Title
Bariatric/Metabolic Surgery Induces Noticeable Changes of Microbiota and Their Secreting Extracellular Vesicle Composition in the Gut
Authors
Yeon-Ju Huh
Joo-Young Seo
Jieun Nam
Jinho Yang
Andrea McDowell
Yoon-Keun Kim
Joo-Ho Lee
Publication date
01-08-2019
Publisher
Springer US
Published in
Obesity Surgery / Issue 8/2019
Print ISSN: 0960-8923
Electronic ISSN: 1708-0428
DOI
https://doi.org/10.1007/s11695-019-03852-1

Other articles of this Issue 8/2019

Obesity Surgery 8/2019 Go to the issue