The human gut microbiome: a review of the effect of obesity and surgically induced weight loss

Timothy E Sweeney, John M Morton, Timothy E Sweeney, John M Morton

Abstract

Recent advances in parallel genomic processing and computational mapping have been applied to the native human microbial environment to provide a new understanding of the role of the microbiome in health and disease. In particular, studies of the distal gut microbiome have proposed that changes in gut microbiota are related to obesity, the metabolic syndrome, and Western diet. We examined the changes in the distal gut microbiome composition as it relates to the lean and obese phenotypes, particularly after surgical weight loss. A PubMed search of publications from January 1, 2005, through December 31, 2012, used the search terms weight, obesity, microbiome, and bariatric surgery. We included studies that provided information on subjects' weight and/or body mass index and a formal assessment of the microbiome. Certain bacteria, specifically the archaeon Methanobrevibacter smithii, have enhanced ability to metabolize dietary substrate, thereby increasing host energy intake and weight gain. With weight loss, there is a decrease in the ratio of Firmicutes to Bacteroidetes phyla. One major finding from microbial sequencing analyses after Roux-en-Y gastric bypass is the comparative overabundance of Proteobacteria in the distal gut microbiome, which is distinct from the changes seen in weight loss without Roux-en-Y gastric bypass. This review provides the practicing surgeon with (1) an update on the state of a rapidly innovating branch of clinical bioinformatics, specifically, the microbiome; (2) a new understanding of the microbiome changes after Roux-en-Y gastric bypass and weight loss; and (3) a basis for understanding further clinical applications of studies of the distal gut microbiome, such as in Crohn disease, ulcerative colitis, and infectious colitis.

References

    1. Luckey TD. Introduction to the ecology of the intestinal flora. Am J Clin Nutr. 1970;23(11):1430–1432.
    1. Fraher MH, O'Toole PW, Quigley EM. Techniques used to characterize the gut microbiota: a guide for the clinician. Nat Rev Gastroenterol Hepatol. 2012;9(6):312–322.
    1. Marguiles M, Egholm M, Altman WE, et al. Genome sequencing in microfabricated high-density picolitre reactors [published correction appears in Nature. 2006;441(7089):120] Nature. 2005;437(7057):376–380.
    1. Gill SR, Pop M, Deboy RT, et al. Metagenomic analysis of the human distal gut microbiome. Science. 2006;312(5778):1355–1359.
    1. Qin J, Li R, Raes J, et al. MetaHIT Consortium A human gut microbial gene catalogue established by metagenomic sequencing. Nature. 2010;464(7285):59–65.
    1. Human Microbiome Project Consortium Structure, function and diversity of the healthy human microbiome. Nature. 2012;486(7402):207–214.
    1. Suau A, Bonnet R, Sutren M, et al. Direct analysis of genes encoding 16S rRNA from complex communities reveals many novel molecular species within the human gut. Appl Environ Microbiol. 1999;65(11):4799–4807.
    1. Arumugam M, Raes J, Pelletier E, et al. MetaHIT Consortium Enterotypes of the human gut microbiome. Nature. 2011;473(7346):174–180.
    1. Turnbaugh PJ, Hamady M, Yatsunenko T, et al. A core gut microbiome in obese and lean twins. Nature. 2009;457(7228):480–484.
    1. Ley RE, Turnbaugh PJ, Klein S, Gordon JI. Microbial ecology: human gut microbes associated with obesity. Nature. 2006;444(7122):1022–1023.
    1. Armougom F, Henry M, Vialettes B, Raccah D, Raoult D. Monitoring bacterial community of human gut microbiota reveals an increase in Lactobacillus in obese patients and Methanogens in anorexic patients. PLoS One. 2009;4(9):e7125. doi:10.1371/journal.pone.0007125.
    1. Balamurugan R, George G, Kabeerdoss J, Hepsiba J, Chandragunasekaran AM, Ramakrishna BS. Quantitative differences in intestinal Faecalibacterium prausnitzii in obese Indian children. Br J Nutr. 2010;103(3):335–338.
    1. Duncan SH, Lobley GE, Holtrop G, et al. Human colonic microbiota associated with diet, obesity and weight loss. Int J Obes (Lond) 2008;32(11):1720–1724.
    1. Ley RE, Baäckhed F, Turnbaugh P, Lozupone CA, Knight RD, Gordon JI. Obesity alters gut microbial ecology. Proc Natl Acad Sci U S A. 2005;102(31):11070–11075.
    1. Nadal I, Santacruz A, Marcos A, et al. Shifts in Clostridia, Bacteroides and immunoglobulin-coating fecal bacteria associated with weight loss in obese adolescents [published correction appears in Int J Obes (Lond). 2012;36(10):1370] Int J Obes (Lond) 2009;33(7):758–767.
    1. Santacruz A, Marcos A, Wärnberg J, et al. EVASYON Study Group Interplay between weight loss and gut microbiota composition in overweight adolescents. Obesity (Silver Spring) 2009;17(10):1906–1915.
    1. Schwiertz A, Taras D, Schaäfer K, et al. Microbiota and SCFA in lean and over-weight healthy subjects. Obesity (Silver Spring) 2010;18(1):190–195.
    1. Turnbaugh PJ, Ley RE, Mahowald MA, Magrini V, Mardis ER, Gordon JI. An obesity-associated gut microbiome with increased capacity for energy harvest. Nature. 2006;444(7122):1027–1031.
    1. Zhang C, Zhang M, Wang S, et al. Interactions between gut microbiota, host genetics and diet relevant to development of metabolic syndromes in mice [published correction appears in ISME J. 2010;4(2):312-313] ISME J. 2010;4(2):232–241.
    1. Turnbaugh PJ, Ridaura VK, Faith JJ, Rey FE, Knight R, Gordon JI. The effect of diet on the human gut microbiome: a metagenomic analysis in humanized gnotobiotic mice. Sci Transl Med. 2009;1(6):6ra14. doi:10.1126/scitranslmed.3000322.
    1. Woodard GA, Encarnacion B, Downey JR, et al. Probiotics improve outcomes after Roux-en-Y gastric bypass surgery: a prospective randomized trial. J Gastrointest Surg. 2009;13(7):1198–1204.
    1. Zhang H, DiBaise JK, Zuccolo A, et al. Human gut microbiota in obesity and after gastric bypass. Proc Natl Acad Sci U S A. 2009;106(7):2365–2370.
    1. Furet JP, Kong LC, Tap J, et al. Differential adaptation of human gut microbiota to bariatric surgery-induced weight loss: links with metabolic and low-grade inflammation markers. Diabetes. 2010;59(12):3049–3057.
    1. Li JV, Ashrafian H, Bueter M, et al. Metabolic surgery profoundly influences gut microbial-host metabolic cross-talk. Gut. 2011;60(9):1214–1223.
    1. Li JV, Reshat R, Wu Q, et al. Experimental bariatric surgery in rats generates a cytotoxic chemical environment in the gut contents. Front Microbiol. 2011;2:183. doi:10.3389/fmicb.2011.00183.
    1. Samuel BS, Gordon JI. A humanized gnotobiotic mouse model of host-archaeal-bacterial mutualism. Proc Natl Acad Sci U S A. 2006;103(26):10011–10016.
    1. Samuel BS, Hansen EE, Manchester JK, et al. Genomic and metabolic adaptations of Methanobrevibacter smithii to the human gut. Proc Natl Acad Sci U S A. 2007;104(25):10643–10648.
    1. Mahowald MA, Rey FE, Seedorf H, et al. Characterizing a model human gut microbiota composed of members of its two dominant bacterial phyla. Proc Natl Acad Sci U S A. 2009;106(14):5859–5864.
    1. Greenblum S, Turnbaugh PJ, Borenstein E. Metagenomic systems biology of the human gut microbiome reveals topological shifts associated with obesity and inflammatory bowel disease. Proc Natl Acad Sci U S A. 2012;109(2):594–599.
    1. Carvalho BM, Guadagnini D, Tsukumo DM, et al. Modulation of gut microbiota by antibiotics improves insulin signalling in high-fat fed mice. Diabetologia. 2012;55(10):2823–2834.
    1. Wikoff WR, Anfora AT, Liu J, et al. Metabolomics analysis reveals large effects of gut microflora on mammalian blood metabolites. Proc Natl Acad Sci U S A. 2009;106(10):3698–3703.

Source: PubMed

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