Impact of diet and individual variation on intestinal microbiota composition and fermentation products in obese men

ISME Journal - Tập 8 Số 11 - Trang 2218-2230 - 2014
Anne Salonen1, Leo Lahti2,3, Jarkko Salojärvi4, Grietje Holtrop5, Katri Korpela1, Sylvia H. Duncan6, Priya Date6, Freda Farquharson6, Alexandra M. Johnstone6, G. E. Lobley6, Petra Louis6, Harry J. Flint6, Willem M. de Vos2,1,3
1Immunobiology Research Program, Department of Bacteriology and Immunology, Haartman Institute, University of Helsinki , Helsinki, Finland
2Department of Veterinary Biosciences, University of Helsinki , HelsinkiFinland
3Laboratory of Microbiology, Wageningen University, Wageningen, The Netherlands
4Department of Veterinary Biosciences, University of Helsinki, Helsinki, Finland
5Biomathematics and Statistics Scotland, Aberdeen, UK
6Rowett Institute of Nutrition and Health, University of Aberdeen, Aberdeen, UK

Tóm tắt

Abstract There is growing interest in understanding how diet affects the intestinal microbiota, including its possible associations with systemic diseases such as metabolic syndrome. Here we report a comprehensive and deep microbiota analysis of 14 obese males consuming fully controlled diets supplemented with resistant starch (RS) or non-starch polysaccharides (NSPs) and a weight-loss (WL) diet. We analyzed the composition, diversity and dynamics of the fecal microbiota on each dietary regime by phylogenetic microarray and quantitative PCR (qPCR) analysis. In addition, we analyzed fecal short chain fatty acids (SCFAs) as a proxy of colonic fermentation, and indices of insulin sensitivity from blood samples. The diet explained around 10% of the total variance in microbiota composition, which was substantially less than the inter-individual variance. Yet, each of the study diets induced clear and distinct changes in the microbiota. Multiple Ruminococcaceae phylotypes increased on the RS diet, whereas mostly Lachnospiraceae phylotypes increased on the NSP diet. Bifidobacteria decreased significantly on the WL diet. The RS diet decreased the diversity of the microbiota significantly. The total 16S ribosomal RNA gene signal estimated by qPCR correlated positively with the three major SCFAs, while the amount of propionate specifically correlated with the Bacteroidetes. The dietary responsiveness of the individual’s microbiota varied substantially and associated inversely with its diversity, suggesting that individuals can be stratified into responders and non-responders based on the features of their intestinal microbiota.

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Tài liệu tham khảo

Bang, 2008, Integrative top-down system metabolic modeling in experimental disease states via data-driven Bayesian methods, J Proteome Res, 7, 497, 10.1021/pr070350l

Becker, 1988, The new S language: a programming environment for data analysis and graphics, Wadsworth and Brooks

Bouhnik, 2006, The capacity of short-chain fructo-oligosaccharides to stimulate faecal bifidobacteria: a dose-response relationship study in healthy humans, Nutr J, 5, 8, 10.1186/1475-2891-5-8

Burcelin, 2012, Immuno-microbiota cross and talk: the new paradigm of metabolic diseases, Sem Immunol, 24, 67, 10.1016/j.smim.2011.11.011

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

Claesson, 2009, Comparative analysis of pyrosequencing and a phylogenetic microarray for exploring microbial community structures in the human distal intestine, PLoS One, 20, e6669, 10.1371/journal.pone.0006669

Claesson, 2012, Gut microbiota composition correlates with diet and health in the elderly, Nature, 488, 178, 10.1038/nature11319

Cotillard, 2013, Dietary intervention impact on gut microbial gene richness, Nature, 500, 585, 10.1038/nature12480

David, 2014, Diet rapidly and reproducibly alters the human gut microbiome, Nature, 505, 559, 10.1038/nature12820

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

Dewulf, 2012, Insight into the prebiotic concept: lessons from an exploratory, double blind intervention study with inulin-type fructans in obese women, Gut, 62, 1112, 10.1136/gutjnl-2012-303304

Duncan, 2007, Reduced dietary intake of carbohydrates by obese subjects results in decreased concentrations of butyrate and butyrate-producing bacteria in feces, Appl Environ Microbiol, 73, 1073, 10.1128/AEM.02340-06

Everard, 2013, Diabetes, obesity and gut microbiota, Best Prac Res Clin Gastroenterol, 27, 73, 10.1016/j.bpg.2013.03.007

FS Teixeira, 2013, Faecal levels of Bifidobacterium and Clostridium coccoides but not plasma lipopolysaccharide are inversely related to insulin and HOMA index in women, Clin Nutr, 32, 1017, 10.1016/j.clnu.2013.02.008

Faith, 2011, Predicting a human gut microbiota’s response to diet in gnotobiotic mice, Science, 333, 101, 10.1126/science.1206025

Flint, 2008, Polysaccharide utilization by gut bacteria: potential for new insights from genomic analysis, Nat Rev Microbiol, 6, 121, 10.1038/nrmicro1817

Flint, 2011, Obesity and the gut microbiota, J Clin Gastroenterol, 45, S128, 10.1097/MCG.0b013e31821f44c4

Flint, 2012, Microbial degradation of complex carbohydrates in the gut, Gut Microbes, 3, 289, 10.4161/gmic.19897

Flint, 2012, The role of the gut microbiota in nutrition and health, Nat Rev Gastroenterol Hepatol, 9, 577, 10.1038/nrgastro.2012.156

Govers, 1999, Wheat bran affects the site of fermentation of resistant starch and luminal indexes related to colon cancer risk: a study in pigs, Gut, 45, 840, 10.1136/gut.45.6.840

Jalanka-Tuovinen, 2011, Intestinal microbiota in healthy adults: temporal analysis reveals individual and common core and relation to intestinal symptoms, PLoS One, 6, e23035, 10.1371/journal.pone.0023035

Korpela, 2014, Gut microbiota signatures predict host and microbiota responses to dietary interventions in obese individuals, PLoS One, 9, e90702, 10.1371/journal.pone.0090702

Lampe, 2013, Inter-individual differences in response to dietary intervention: integrating omics platforms towards personalised dietary recommendation, Proc Nutr Soc, 72, 207, 10.1017/S0029665113000025

Lappi, 2013, Intake of whole-grain and fiber-rich rye bread versus refined wheat bread does not differentiate intestinal microbiota composition in finnish adults with metabolic syndrome, J Nutr, 143, 648, 10.3945/jn.112.172668

Lobley, 2013, Impact of short term consumption of diets high in either non-starch polysaccharides or resistant starch in comparison with moderate weight loss on indices of insulin sensitivity in subjects with metabolic syndrome, Nutrients, 5, 2144, 10.3390/nu5062144

Macfarlane, 2011, Fermentation in the human large intestine: its physiologic consequences and the potential contribution of prebiotics, J Clin Gastroenterol, 45, S120, 10.1097/MCG.0b013e31822fecfe

Martínez, 2010, Resistant starches types 2 and 4 have differential effects on the composition of the fecal microbiota in human subjects, PLoS One, 5, e15046, 10.1371/journal.pone.0015046

Martínez, 2012, Gut microbiome composition is linked to whole grain-induced immunological improvements, ISME J, 7, 269, 10.1038/ismej.2012.104

Qin, 2010, A human gut microbial gene catalogue established by metagenomic sequencing, Nature, 464, 59, 10.1038/nature08821

Rajilić-Stojanović, 2009, Development and application of the human intestinal tract chip, a phylogenetic microarray: analysis of universally conserved phylotypes in the abundant microbiota of young and elderly adults, Environ Microbiol, 11, 1736, 10.1111/j.1462-2920.2009.01900.x

Ramirez-Farias, 2009, Effect of inulin on the human gut microbiota: stimulation of Bifidobacterium adolescentis and Faecalibacterium prausnitzii, Br J Nutr, 101, 541, 10.1017/S0007114508019880

Richardson, 1989, Simultaneous determination of volatile and non-volatile acidic fermentation products of anaerobes by capillary gas chromatography, Lett Appl Microbiol, 9, 5, 10.1111/j.1472-765X.1989.tb00278.x

Russell, 2011, High-protein, reduced-carbohydrate weight-loss diets promote metabolite profiles likely to be detrimental to colonic health, Am J Clin Nutr, 93, 1062, 10.3945/ajcn.110.002188

Russell, 2013, Colonic bacterial metabolites and human health, Curr Opin Microbiol, 16, 246, 10.1016/j.mib.2013.07.002

Salonen, 2010, Comparative analysis of fecal DNA extraction methods with phylogenetic microarray: effective recovery of bacterial and archaeal DNA using mechanical cell lysis, J Microbioll Methods, 81, 127, 10.1016/j.mimet.2010.02.007

The Human Microbiome Project Consortium, 2012, Structure, function and diversity of the healthy human microbiome, Nature, 486, 207, 10.1038/nature11234

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

10.1111/1462-2920.12217

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

Yang, 2013, In vitro characterization of the impact of selected dietary fibers on fecal microbiota composition and short chain fatty acid production, Anaerobe, 23C, 74, 10.1016/j.anaerobe.2013.06.012

Yatsunenko, 2012, Human gut microbiome viewed across age and geography, Nature, 486, 222, 10.1038/nature11053

Ze, 2012, Ruminococcus bromii is a keystone species for the degradation of resistant starch in the human colon, ISME J, 6, 1535, 10.1038/ismej.2012.4

Zhang, 2009, Interactions between gut microbiota, host genetics and diet relevant to development of metabolic syndromes in mice, ISME J, 4, 232, 10.1038/ismej.2009.112