Structural resilience of the gut microbiota in adult mice under high-fat dietary perturbations

ISME Journal - Tập 6 Số 10 - Trang 1848-1857 - 2012
Chenhong Zhang1, Menghui Zhang1, Xiaoyan Pang1, Yufeng Zhao2, Linghua Wang1, Liping Zhao2,1
1State Key Laboratory of Microbial Metabolism, School of Life Sciences and Biotechnology, Shanghai Jiao Tong University, Shanghai, China
2Ministry of Education Key Laboratory of Systems Biomedicine, Shanghai Centre for Systems Biomedicine , Shanghai , China

Tóm tắt

Abstract Disruption of the gut microbiota by high-fat diet (HFD) has been implicated in the development of obesity. It remains to be elucidated whether the HFD-induced shifts occur at the phylum level or whether they can be attributed to specific phylotypes; additionally, it is unclear to what extent the changes are reversible under normal chow (NC) feeding. One group (diet-induced obesity, DIO) of adult C57BL/6J mice was fed a HFD for 12 weeks until significant obesity and insulin resistance were observed, and then these mice were switched to NC feeding for 10 weeks. Upon switching to NC feeding, the metabolic deteriorations observed during HFD consumption were significantly alleviated. The second group (control, CHO) remained healthy under continuous NC feeding. UniFrac analysis of bar-coded pyrosequencing data showed continued structural segregation of DIO from CHO on HFD. At 4 weeks after switching back to NC, the gut microbiota in the DIO group had already moved back to the CHO space, and continued to progress along the same age trajectory and completely converged with CHO after 10 weeks. Redundancy analysis identified 77 key phylotypes responding to the dietary perturbations. HFD-induced shifts of these phylotypes all reverted to CHO levels over time. Some of these phylotypes exhibited robust age-related changes despite the dramatic abundance variations in response to dietary alternations. These findings suggest that HFD-induced structural changes of the gut microbiota can be attributed to reversible elevation or diminution of specific phylotypes, indicating the significant structural resilience of the gut microbiota of adult mice to dietary perturbations.

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Tài liệu tham khảo

Akhaddar, 2002, Cerebellar abscess due to lactococcus lactis. A new pathogen, Acta Neurochir, 144, 305, 10.1007/s007010200041

Beerens, 1977, Sulfate-reducing anaerobic bacteria in human feces, Am J Clin Nutr, 30, 1770, 10.1093/ajcn/30.11.1770

Biagi, 2010, Through ageing, and beyond: gut microbiota and inflammatory status in seniors and centenarians, PLoS One, 5, e10667, 10.1371/journal.pone.0010667

Cani, 2008, Changes in gut microbiota control metabolic endotoxemia-induced inflammation in high-fat diet-induced obesity and diabetes in mice, Diabetes, 57, 1470, 10.2337/db07-1403

Cani, 2007, Selective increases of bifidobacteria in gut microflora improve high-fat-diet-induced diabetes in mice through a mechanism associated with endotoxaemia, Diabetologia, 50, 2374, 10.1007/s00125-007-0791-0

Cani, 2009, Changes in gut microbiota control inflammation in obese mice through a mechanism involving GLP-2-driven improvement of gut permeability, Gut, 58, 1091, 10.1136/gut.2008.165886

De Filippo, 2010, Impact of diet in shaping gut microbiota revealed by a comparative study in children from Europe and rural Africa, Proc Natl Acad Sci USA, 107, 14691, 10.1073/pnas.1005963107

DeSantis, 2006, NAST: a multiple sequence alignment server for comparative analysis of 16S rRNA genes, Nucleic Acids Res, 34, W394, 10.1093/nar/gkl244

Dethlefsen, 2010, Microbes and Health Sackler Colloquium: Incomplete recovery and individualized responses of the human distal gut microbiota to repeated antibiotic perturbation, Proc Natl Acad Sci USA, 108, 4554, 10.1073/pnas.1000087107

Duncan, 2008, Human colonic microbiota associated with diet, obesity and weight loss, Int J Obes, 32, 1720, 10.1038/ijo.2008.155

Flint, 2007, Interactions and competition within the microbial community of the human colon: links between diet and health, Environ Microbiol, 9, 1101, 10.1111/j.1462-2920.2007.01281.x

Griffiths, 2004, In vivo effects of bifidobacteria and lactoferrin on gut endotoxin concentration and mucosal immunity in Balb/c mice, Dig Dis Sci, 49, 579, 10.1023/B:DDAS.0000026302.92898.ae

Guigoz, 2008, The inflammatory status of old age can be nurtured from the intestinal environment, Curr Opin Clin Nutr Metab Care, 11, 13, 10.1097/MCO.0b013e3282f2bfdf

Hopkins, 2002, Changes in predominant bacterial populations in human faeces with age and with Clostridium difficile infection, J Med Microbiol, 51, 448, 10.1099/0022-1317-51-5-448

Jia, 2008, Gut microbiota: a potential new territory for drug targeting, Nat Rev, 7, 123

Kleessen, 1997, Effects of inulin and lactose on fecal microflora, microbial activity, and bowel habit in elderly constipated persons, Am J Clin Nutr, 65, 1397, 10.1093/ajcn/65.5.1397

Ley, 2005, Obesity alters gut microbial ecology, Proc Natl Acad Sci USA, 102, 11070, 10.1073/pnas.0504978102

Ley, 2006, Ecological and evolutionary forces shaping microbial diversity in the human intestine, Cell, 124, 837, 10.1016/j.cell.2006.02.017

Ley, 2006, Microbial ecology: human gut microbes associated with obesity, Nature, 444, 1022, 10.1038/4441022a

Loubinoux, 2000, Bacteremia caused by a strain of desulfovibrio related to the provisionally named desulfovibrio fairfieldensis, J Clin Microbiol, 38, 931, 10.1128/JCM.38.2.931-934.2000

Ludwig, 2004, ARB: a software environment for sequence data, Nucleic Acids Res, 32, 1363, 10.1093/nar/gkh293

Margulies, 2005, Genome sequencing in microfabricated high-density picolitre reactors, Nature, 437, 376, 10.1038/nature03959

Mariat, 2009, The Firmicutes/Bacteroidetes ratio of the human microbiota changes with age, BMC Microbiol, 9, 123, 10.1186/1471-2180-9-123

McKenna, 2008, The macaque gut microbiome in health, lentiviral infection, and chronic enterocolitis, PLoS Pathog, 4, e20, 10.1371/journal.ppat.0040020

Michalski, 2006, Human inflammatory bowel disease does not associate with Lawsonia intracellularis infection, BMC Microbiol, 6, 81, 10.1186/1471-2180-6-81

Mitsuoka, 1992, Intestinal flora and aging, Nutr Rev, 50, 438, 10.1111/j.1753-4887.1992.tb02499.x

Mosca, 1995, Preliminary evidence of endotoxic activity of Bilophila wadsworthia, Anaerobe, 1, 21, 10.1016/S1075-9964(95)80379-3

Mueller, 2006, Differences in fecal microbiota in different European study populations in relation to age, gender, and country: a cross-sectional study, Appl Environ Microbiol, 72, 1027, 10.1128/AEM.72.2.1027-1033.2006

Murphy, 2010, Composition and energy harvesting capacity of the gut microbiota: relationship to diet, obesity and time in mouse models, Gut, 59, 1635, 10.1136/gut.2010.215665

Muyzer, 1993, Profiling of complex microbial populations by denaturing gradient gel electrophoresis analysis of polymerase chain reaction-amplified genes coding for 16S rRNA, Appl Environ Microbiol, 59, 695, 10.1128/aem.59.3.695-700.1993

Ostan, 2008, Immunosenescence and immunogenetics of human longevity, Neuroimmunomodulation, 15, 224, 10.1159/000156466

Popkin, 2007, The World is Fat: The Fads, Trends, Policies, and Products That Are Fattening the Human Race, 10.1038/scientificamerican0907-88

Schloss, 2005, Introducing DOTUR, a computer program for defining operational taxonomic units and estimating species richness, Appl Environ Microbiol, 71, 1501, 10.1128/AEM.71.3.1501-1506.2005

Schwiertz, 2010, Microbiota and SCFA in lean and overweight healthy subjects, Obesity, 18, 190, 10.1038/oby.2009.167

Sogin, 2006, Microbial diversity in the deep sea and the underexplored “rare biosphere”, Proc Natl Acad Sci USA, 103, 12115, 10.1073/pnas.0605127103

Sonnenburg, 2004, Getting a grip on things: how do communities of bacterial symbionts become established in our intestine?, Nat Immunol, 5, 569, 10.1038/ni1079

Turnbaugh, 2008, Diet-induced obesity is linked to marked but reversible alterations in the mouse distal gut microbiome, Cell Host Microbe, 3, 213, 10.1016/j.chom.2008.02.015

Turnbaugh, 2009, A core gut microbiome in obese and lean twins, Nature, 457, 480, 10.1038/nature07540

Turnbaugh, 2006, An obesity-associated gut microbiome with increased capacity for energy harvest, Nature, 444, 1027, 10.1038/nature05414

Walker, 2011, Dominant and diet-responsive groups of bacteria within the human colonic microbiota, ISMEJ, 5, 220, 10.1038/ismej.2010.118

Wang, 2006, The role of bifidobacteria in gut barrier function after thermal injury in rats, J Trauma, 61, 650, 10.1097/01.ta.0000196574.70614.27

Wang, 2004, Risk factors of development of gut-derived bacterial translocation in thermally injured rats, World J Gastroenterol, 10, 1619, 10.3748/wjg.v10.i11.1619

Weglarz, 2003, Desulfovibrio desulfuricans lipopolysaccharides induce endothelial cell IL-6 and IL-8 secretion and E-selectin and VCAM-1 expression, Cell Mol Biol Lett, 8, 991

Woodmansey, 2004, Comparison of compositions and metabolic activities of fecal microbiotas in young adults and in antibiotic-treated and non-antibiotic-treated elderly subjects, Appl Environ Microbiol, 70, 6113, 10.1128/AEM.70.10.6113-6122.2004

Wu, 2011, Linking long-term dietary patterns with gut microbial enterotypes, Science, 334, 105, 10.1126/science.1208344

Zhang, 2010, Interactions between gut microbiota, host genetics and diet relevant to development of metabolic syndromes in mice, ISMEJ, 4, 232, 10.1038/ismej.2009.112