The gut microbiota of Colombians differs from that of Americans, Europeans and Asians

Juan S Escobar, Bernadette Klotz, Beatriz E Valdes, Gloria M Agudelo, Juan S Escobar, Bernadette Klotz, Beatriz E Valdes, Gloria M Agudelo

Abstract

Background: The composition of the gut microbiota has recently been associated with health and disease, particularly with obesity. Some studies suggested a higher proportion of Firmicutes and a lower proportion of Bacteroidetes in obese compared to lean people; others found discordant patterns. Most studies, however, focused on Americans or Europeans, giving a limited picture of the gut microbiome. To determine the generality of previous observations and expand our knowledge of the human gut microbiota, it is important to replicate studies in overlooked populations. Thus, we describe here, for the first time, the gut microbiota of Colombian adults via the pyrosequencing of the 16S ribosomal DNA (rDNA), comparing it with results obtained in Americans, Europeans, Japanese and South Koreans, and testing the generality of previous observations concerning changes in Firmicutes and Bacteroidetes with increasing body mass index (BMI).

Results: We found that the composition of the gut microbiota of Colombians was significantly different from that of Americans, Europeans and Asians. The geographic origin of the population explained more variance in the composition of this bacterial community than BMI or gender. Concerning changes in Firmicutes and Bacteroidetes with obesity, in Colombians we found a tendency in Firmicutes to diminish with increasing BMI, whereas no change was observed in Bacteroidetes. A similar result was found in Americans. A more detailed inspection of the Colombian dataset revealed that five fiber-degrading bacteria, including Akkermansia, Dialister, Oscillospira, Ruminococcaceae and Clostridiales, became less abundant in obese subjects.

Conclusion: We contributed data from unstudied Colombians that showed that the geographic origin of the studied population had a greater impact on the composition of the gut microbiota than BMI or gender. Any strategy aiming to modulate or control obesity via manipulation of this bacterial community should consider this effect.

Figures

Figure 1
Figure 1
Taxonomic profiles of the gut microbiota of Colombians and Americans. (A) Relative abundance of phylum-level OTUs. (B) Relative abundance of the most frequent genus-level OTUs (frequency >0.5%), colored by their respective phylum (see Figure A). Unclassified phylotypes are marked with asterisk. Upper bars = Colombians; lower bars = Americans.
Figure 2
Figure 2
Principal correspondence analysis of UniFrac distances. Differences in the composition of the gut microbiota according to the geographic origin of the sampled population (A), nutritional status (B) and gender (C). R2 and P-value from permutational multivariate analysis of variance (adonis function).
Figure 3
Figure 3
Changes in the abundance of phylum-level and genus-level OTUs with BMI in the Colombian dataset. A-B: phylum-level OTUs; C-G: genus-level OTUs. Background color: green = lean; yellow = overweight; red = obese. Pearson’s r from correlation analyses and P-value from linear models.

References

    1. The Human Microbiome Project Consortium Structure, function and diversity of the healthy human microbiome. Nature. 2012;486:207–214. doi: 10.1038/nature11234.
    1. Pray L, Pillsbury L, Tomayko E. The Human Microbiome, Diet, and Health: Workshop Summary. Washington, D. C.: National Academy of Sciences; 2012.
    1. Eckburg PB, Bik EM, Bernstein CN, Purdom E, Dethlefsen L, Sargent M, Gill SR, Nelson KE, Relman DA. Diversity of the human intestinal microbial flora. Science. 2005;308:1635–1638. doi: 10.1126/science.1110591.
    1. Backhed F, Ley RE, Sonnenburg JL, Peterson DA, Gordon JI. Host-bacterial mutualism in the human intestine. Science. 2005;307:1915–1920. doi: 10.1126/science.1104816.
    1. Guarner F, Malagelada JR. Gut flora in health and disease. Lancet. 2003;361:512–519. doi: 10.1016/S0140-6736(03)12489-0.
    1. Mazmanian SK, Liu CH, Tzianabos AO, Kasper DL. An immunomodulatory molecule of symbiotic bacteria directs maturation of the host immune system. Cell. 2005;122:107–118. doi: 10.1016/j.cell.2005.05.007.
    1. Backhed F, Ding H, Wang T, Hooper LV, Koh GY, Nagy A, Semenkovich CF, Gordon JI. The gut microbiota as an environmental factor that regulates fat storage. Proc Natl Acad Sci U S A. 2004;101:15718–15723. doi: 10.1073/pnas.0407076101.
    1. Ley RE. Obesity and the human microbiome. Curr Opin Gastroenterol. 2010;26:5–11. doi: 10.1097/MOG.0b013e328333d751.
    1. Wen L, Ley RE, Volchkov PY, Stranges PB, Avanesyan L, Stonebraker AC, Hu C, Wong FS, Szot GL, Bluestone JA, Gordon JI, Chervonsky AV. Innate immunity and intestinal microbiota in the development of Type 1 diabetes. Nature. 2008;455:1109–1113. doi: 10.1038/nature07336.
    1. Larsen N, Vogensen FK, van den Berg FW, Nielsen DS, Andreasen AS, Pedersen BK, Al-Soud WA, Sorensen SJ, Hansen LH, Jakobsen M. Gut microbiota in human adults with type 2 diabetes differs from non-diabetic adults. PLoS One. 2010;5:e9085. doi: 10.1371/journal.pone.0009085.
    1. Mai V, Colbert LH, Perkins SN, Schatzkin A, Hursting SD. Intestinal microbiota: a potential diet-responsive prevention target in ApcMin mice. Mol Carcinog. 2007;46:42–48. doi: 10.1002/mc.20233.
    1. Clarke SF, Murphy EF, Nilaweera K, Ross PR, Shanahan F, O’Toole PW, Cotter PD. The gut microbiota and its relationship to diet and obesity: new insights. Gut Microbes. 2012;3:186–202. doi: 10.4161/gmic.20168.
    1. Scott KP, Gratz SW, Sheridan PO, Flint HJ, Duncan SH: The influence of diet on the gut microbiota.Pharmacol Res 2012. In press
    1. Cox LM, Blaser MJ. Pathways in microbe-induced obesity. Cell Metab. 2013;17:883–894. doi: 10.1016/j.cmet.2013.05.004.
    1. Turnbaugh PJ, Backhed F, Fulton L, Gordon JI. Diet-induced obesity is linked to marked but reversible alterations in the mouse distal gut microbiome. Cell Host Microbe. 2008;3:213–223. doi: 10.1016/j.chom.2008.02.015.
    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;444:1027–1031. doi: 10.1038/nature05414.
    1. Ley RE, Backhed F, Turnbaugh P, Lozupone CA, Knight RD, Gordon JI. Obesity alters gut microbial ecology. Proc Natl Acad Sci U S A. 2005;102:11070–11075. doi: 10.1073/pnas.0504978102.
    1. Murphy EF, Cotter PD, Healy S, Marques TM, O’Sullivan O, Fouhy F, Clarke SF, O’Toole PW, Quigley EM, Stanton C, Ross PR, O’Doherty RM, Shanahan F. Composition and energy harvesting capacity of the gut microbiota: relationship to diet, obesity and time in mouse models. Gut. 2010;59:1635–1642. doi: 10.1136/gut.2010.215665.
    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;1:6ra–14ra. doi: 10.1126/scitranslmed.3000322.
    1. Ley RE, Turnbaugh PJ, Klein S, Gordon JI. Microbial ecology: human gut microbes associated with obesity. Nature. 2006;444:1022–1023. doi: 10.1038/4441022a.
    1. Collado MC, Isolauri E, Laitinen K, Salminen S. Distinct composition of gut microbiota during pregnancy in overweight and normal-weight women. Am J Clin Nutr. 2008;88:894–899.
    1. Duncan SH, Lobley GE, Holtrop G, Ince J, Johnstone AM, Louis P, Flint HJ. Human colonic microbiota associated with diet, obesity and weight loss. Int J Obes (Lond) 2008;32:1720–1724. doi: 10.1038/ijo.2008.155.
    1. Ismail NA, Ragab SH, ElBaky AA, Shoeib ARS, Alhosary Y, Fekry D. Frequency of Firmicutes and Bacteroidetes in gut microbiota in obese and normal weight Egyptian children and adults. Archives of Med Sci. 2011;7:501–507. doi: 10.5114/aoms.2011.23418.
    1. Schwiertz A, Taras D, Schafer K, Beijer S, Bos NA, Donus C, Hardt PD. Microbiota and SCFA in lean and overweight healthy subjects. Obesity. 2010;18:190–195. doi: 10.1038/oby.2009.167.
    1. Tims S, Derom C, Jonkers DM, Vlietinck R, Saris WH, Kleerebezem M, de Vos WM, Zoetendal EG. Microbiota conservation and BMI signatures in adult monozygotic twins. ISME J. 2012;7:707–717. doi: 10.1038/ismej.2012.146.
    1. Qin J, Li R, Raes J, Arumugam M, Burgdorf KS, Manichanh C, Nielsen T, Pons N, Levenez F, Yamada T, Mende DR, Li J, Xu J, Li S, Li D, Cao J, Wang B, Liang H, Zheng H, Xie Y, Tap J, Lepage P, Bertalan M, Batto JM, Hansen T, Le Paslier D, Linneberg A, Nielsen HB, Pelletier E, Renault P. A human gut microbial gene catalogue established by metagenomic sequencing. Nature. 2010;464:59–65. doi: 10.1038/nature08821.
    1. Arumugam M, Raes J, Pelletier E, Le Paslier D, Yamada T, Mende DR, Fernandes GR, Tap J, Bruls T, Batto JM, Bertalan M, Borruel N, Casellas F, Fernandez L, Gautier L, Hansen T, Hattori M, Hayashi T, Kleerebezem M, Kurokawa K, Leclerc M, Levenez F, Manichanh C, Nielsen HB, Nielsen T, Pons N, Poulain J, Qin J, Sicheritz-Ponten T, Tims S, et al. Enterotypes of the human gut microbiome. Nature. 2011;473:174–180. doi: 10.1038/nature09944.
    1. Mueller S, Saunier K, Hanisch C, Norin E, Alm L, Midtvedt T, Cresci A, Silvi S, Orpianesi C, Verdenelli MC, Clavel T, Koebnick C, Zunft HJF, Doré J, Blaut M. Differences in fecal microbiota in different European study populations in relation to age, gender, and country: a cross-sectional study. Appl Environ Microbiol. 2006;72:1027–1033. doi: 10.1128/AEM.72.2.1027-1033.2006.
    1. Lay C, Rigottier-Gois L, Holmstrom K, Rajilic M, Vaughan EE, de Vos WM, Collins MD, Thiel R, Namsolleck P, Blaut M, Dore J. Colonic microbiota signatures across five northern European countries. Appl Environ Microbiol. 2005;71:4153–4155. doi: 10.1128/AEM.71.7.4153-4155.2005.
    1. Schloissnig S, Arumugam M, Sunagawa S, Mitreva M, Tap J, Zhu A, Waller A, Mende DR, Kultima JR, Martin J, Kota K, Sunyaev SR, Weinstock GM, Bork P. Genomic variation landscape of the human gut microbiome. Nature. 2013;493:45–50. doi: 10.1038/nature11711.
    1. Yatsunenko T, Rey FE, Manary MJ, Trehan I, Dominguez-Bello MG, Contreras M, Magris M, Hidalgo G, Baldassano RN, Anokhin AP, Heath AC, Warner B, Reeder J, Kuczynski J, Caporaso JG, Lozupone CA, Lauber C, Clemente JC, Knights D, Knight R, Gordon JI. Human gut microbiome viewed across age and geography. Nature. 2012;486:222–227.
    1. Schnorr SL, Candela M, Rampelli S, Centanni M, Consolandi C, Basaglia G, Turroni S, Biagi E, Peano C, Severgnini M, Fiori J, Gotti R, De Bellis G, Luiselli D, Brigidi P, Mabulla A, Marlowe F, Henry AG, Crittenden AN. Gut microbiome of the Hadza hunter-gatherers. Nat Commun. 2014;5:3654. doi: 10.1038/ncomms4654.
    1. De Filippo C, Cavalieri D, Di Paola M, Ramazzotti M, Poullet JB, Massart S, Collini S, Pieraccini G, Lionetti P. Impact of diet in shaping gut microbiota revealed by a comparative study in children from Europe and rural Africa. Proc Natl Acad Sci U S A. 2010;107:14691–14696. doi: 10.1073/pnas.1005963107.
    1. Suzuki TA, Worobey M. Geographical variation of human gut microbial composition. Biol Lett. 2014;10:20131037. doi: 10.1098/rsbl.2013.1037.
    1. Mai V, McCrary QM, Sinha R, Glei M. Associations between dietary habits and body mass index with gut microbiota composition and fecal water genotoxicity: an observational study in African American and Caucasian American volunteers. Nutritional J. 2009;8:49.
    1. Cox LM, Cho I, Young SA, Anderson WH, Waters BJ, Hung SC, Gao Z, Mahana D, Bihan M, Alekseyenko AV, Methé BA, Blaser MJ. The nonfermentable dietary fiber hydroxypropyl methylcellulose modulates intestinal microbiota. FASEB J. 2013;27:692–702. doi: 10.1096/fj.12-219477.
    1. Faith JJ, McNulty NP, Rey FE, Gordon JI. Predicting a human gut microbiota’s response to diet in gnotobiotic mice. Science. 2011;333:101–104. doi: 10.1126/science.1206025.
    1. Cotillard A, Kennedy SP, Kong LC, Prifti E, Pons N, Le Chatelier E, Almeida M, Quinquis B, Levenez F, Galleron N, Gougis S, Rizkalla S, Batto JM, Renault P, Doré J, Zucker JD, Clément K, Ehrlich SD, ANR MicroObes consortium Dietary intervention impact on gut microbial gene richness. Nature. 2013;500:585–588. doi: 10.1038/nature12480.
    1. David LA, Maurice CF, Carmody RN, Gootenberg DB, Button JE, Wolfe BE, Ling AV, Devlin AS, Varma Y, Fischbach MA, Biddinger SB, Dutton RJ, Turnbaugh PJ. Diet rapidly and reproducibly alters the human gut microbiome. Nature. 2014;505:559–563. doi: 10.1038/nature12820.
    1. Zoetendal EG, Akkermans ADL, Akkermans-van Vliet WM, de Visser JAGM, de Vos WM. The host genotype affects the bacterial community in the human gastrointestinal tract. Microbial Ecology Health Dis. 2001;13:129–134. doi: 10.1080/089106001750462669.
    1. Turnbaugh PJ, Hamady M, Yatsunenko T, Cantarel BL, Duncan A, Ley RE, Sogin ML, Jones WJ, Roe BA, Affourtit JP, Egholm M, Henrissat B, Heath AC, Knight R, Gordon JI. A core gut microbiome in obese and lean twins. Nature. 2009;457:480–487. doi: 10.1038/nature07540.
    1. Claesson MJ, Cusack S, O’Sullivan O, Greene-Diniz R, de Weerd H, Flannery E, Marchesi JR, Falush D, Dinan T, Fitzgerald G, Stanton C, van Sinderen D, O’Connor M, Harnedy N, O’Connor K, Henry C, O’Mahony D, Fitzgerald AP, Shanahan D, Twomey C, Hill C, Ross RP, O’Toole PW. Composition, variability, and temporal stability of the intestinal microbiota of the elderly. Proc Natl Acad Sci U S A. 2011;108:4586–4591. doi: 10.1073/pnas.1000097107.
    1. Palmer C, Bik EM, DiGiulio DB, Relman DA, Brown PO. Development of the human infant intestinal microbiota. PLoS Biol. 2007;5:e177. doi: 10.1371/journal.pbio.0050177.
    1. Antonopoulos DA, Huse SM, Morrison HG, Schmidt TM, Sogin ML, Young VB. Reproducible community dynamics of the gastrointestinal microbiota following antibiotic perturbation. Infect Immun. 2009;77:2367–2375. doi: 10.1128/IAI.01520-08.
    1. Dethlefsen L, Huse S, Sogin ML, Relman DA. The pervasive effects of an antibiotic on the human gut microbiota, as revealed by deep 16S rRNA sequencing. PLoS Biol. 2008;6:e280. doi: 10.1371/journal.pbio.0060280.
    1. Ubeda C, Pamer EG. Antibiotics, microbiota, and immune defense. Trends Immunol. 2012;33:459–466. doi: 10.1016/j.it.2012.05.003.
    1. Jernberg C, Lofmark S, Edlund C, Jansson JK. Long-term ecological impacts of antibiotic administration on the human intestinal microbiota. ISME J. 2007;1:56–66. doi: 10.1038/ismej.2007.3.
    1. Biasucci G, Rubini M, Riboni S, Morelli L, Bessi E, Retetangos C. Mode of delivery affects the bacterial community in the newborn gut. Early Hum Dev. 2010;86:13–15. doi: 10.1016/j.earlhumdev.2010.01.004.
    1. Dominguez-Bello MG, Costello EK, Contreras M, Magris M, Hidalgo G, Fierer N, Knight R. Delivery mode shapes the acquisition and structure of the initial microbiota across multiple body habitats in newborns. Proc Natl Acad Sci U S A. 2010;107:11971–11975. doi: 10.1073/pnas.1002601107.
    1. Huurre A, Kalliomaki M, Rautava S, Rinne M, Salminen S, Isolauri E. Mode of delivery - effects on gut microbiota and humoral immunity. Neonatology. 2008;93:236–240. doi: 10.1159/000111102.
    1. Pandey PK, Verma P, Kumar H, Bavdekar A, Patole MS, Shouche YS. Comparative analysis of fecal microflora of healthy full-term Indian infants born with different methods of delivery (vaginal vs cesarean): Acinetobacter sp. prevalence in vaginally born infants. J Biosci. 2012;37:989–998. doi: 10.1007/s12038-012-9268-5.
    1. Nermes M, Niinivirta K, Nylund L, Laitinen K, Matomäki J, Salminen S, Isolauri E. Perinatal pet exposure, faecal microbiota, and wheezy bronchitis: is there a connection? ISRN Allergy. 2013;2013:827934. doi: 10.1155/2013/827934.
    1. Song SJ, Lauber C, Costello EK, Lozupone CA, Humphrey G, Berg-Lyons D, Caporaso JG, Knights D, Clemente JC, Nakielny S, Gordon JI, Fierer N, Knight R. Cohabiting family members share microbiota with one another and with their dogs. eLife. 2013;2:e00458.
    1. Rojas W, Parra MV, Campo O, Caro MA, Lopera JG, Arias W, Duque C, Naranjo A, Garcia J, Vergara C, Lopera J, Hernandez E, Valencia A, Caicedo Y, Cuartas M, Gutiérrez J, López S, Ruiz-Linares A, Bedoya G. Genetic make up and structure of Colombian populations by means of uniparental and biparental DNA markers. Am J Phys Anthropol. 2010;143:13–20. doi: 10.1002/ajpa.21270.
    1. Moreno-Estrada A, Gravel S, Zakharia F, McCauley JL, Byrnes JK, Gignoux CR, Ortiz-Tello PA, Martínez RJ, Hedges DJ, Morris RW, Eng C, Sandoval K, Acevedo-Acevedo S, Norman PJ, Layrisse Z, Parham P, Martínez-Cruzado JC, González Burchard E, Cuccaro ML, Martin ER, Bustamante CD. Reconstructing the population genetic history of the Caribbean. PLoS Genet. 2013;9:e1003925. doi: 10.1371/journal.pgen.1003925.
    1. Gravel S, Zakharia F, Moreno-Estrada A, Byrnes JK, Muzzio M, Rodriguez-Flores JL, Kenny EE, Gignoux CR, Maples BK, Guiblet W, Dutil J, Via M, Sandoval K, Bedoya G, Oleksyk TK, Ruiz-Linares A, Burchard EG, Martinez-Cruzado JC, Bustamante CD, The 1000 Genomes Project Reconstructing Native American migrations from whole-genome and whole-exome data. PLoS Genet. 2013;9:e1004023. doi: 10.1371/journal.pgen.1004023.
    1. Profamilia Colombia, Instituto Nacional de Salud, Universidad de Antioquia, Organización Panamericana de la Salud, Instituto Colombiano de Bienestar Familiar . Encuesta Nacional de la Situación Nutricional en Colombia, 2005. Bogotá: Instituto Colombiano de Bienestar Familiar; 2006. p. 445.
    1. Profamilia, Instituto Nacional de Salud, Instituto Colombiano de Bienestar Familiar, Ministerio de la Protección Social, Coldeportes, Organización Panamericana de la Salud, Programa Mundial de Alimentos, Departamento Administrativo Nacional de Estadística, Asociación Colombiana de Facultades de Nutrición y Dietética . Encuesta Nacional de la Situación Nutricional en Colombia 2010 ENSIN. Bogotá: Instituto Colombiano de Bienestar Familiar; 2011. p. 509.
    1. Duncan SH, Belenguer A, Holtrop G, Johnstone AM, Flint HJ, Lobley GE. Reduced dietary intake of carbohydrates by obese subjects results in decreased concentrations of butyrate and butyrate-producing bacteria in feces. Appl Environ Microbiol. 2007;73:1073–1078. doi: 10.1128/AEM.02340-06.
    1. Zhang H, DiBaise JK, Zuccolo A, Kudrna D, Braidotti M, Yu Y, Parameswaran P, Crowell MD, Wing R, Rittmann BE, Krajmalnik-Brown R. Human gut microbiota in obesity and after gastric bypass. Proc Natl Acad Sci U S A. 2009;106:2365–2370. doi: 10.1073/pnas.0812600106.
    1. Walker AW, Ince J, Duncan SH, Webster LM, Holtrop G, Ze X, Brown D, Stares MD, Scott P, Bergerat A, Louis P, McIntosh F, Johnstone AM, Lobley GE, Parkhill J, Flint HJ. Dominant and diet-responsive groups of bacteria within the human colonic microbiota. ISME J. 2011;5:220–230. doi: 10.1038/ismej.2010.118.
    1. Nam YD, Jung MJ, Roh SW, Kim MS, Bae JW. Comparative analysis of Korean human gut microbiota by barcoded pyrosequencing. PLoS One. 2011;6:e22109. doi: 10.1371/journal.pone.0022109.
    1. Lohman TG, Roche AF, Martorell R. Anthropometric Standardization Reference Manual. Champaign, IL: Human Kinetics Books; 1988.
    1. Gontcharova VYE, Wolcott RD, Hollister EB, Gentry TJ, Dowd SE. Black Box Chimera Check (B2C2): a windows-based software for batch depletion of chimeras from bacterial 16S rRNA gene datasets. Open Microbiol J. 2010;4:6.
    1. Edgar RC. Search and clustering orders of magnitude faster than BLAST. Bioinformatics. 2010;26:2460–2461. doi: 10.1093/bioinformatics/btq461.
    1. Caporaso JG, Bittinger K, Bushman FD, DeSantis TZ, Andersen GL, Knight R. PyNAST: a flexible tool for aligning sequences to a template alignment. Bioinformatics. 2010;26:266–267. doi: 10.1093/bioinformatics/btp636.
    1. DeSantis TZ, Hugenholtz P, Larsen N, Rojas M, Brodie EL, Keller K, Huber T, Dalevi D, Hu P, Andersen GL. Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Appl Environ Microbiol. 2006;72:5069–5072. doi: 10.1128/AEM.03006-05.
    1. Wang Q, Garrity GM, Tiedje JM, Cole JR. Naïve bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol. 2007;73:5261–5267. doi: 10.1128/AEM.00062-07.
    1. Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Gonzalez Pena A, Goodrich JK, Gordon JI, Huttley GA, Kelley ST, Knights D, Koenig JE, Ley RE, Lozupone CA, McDonald D, Muegge BD, Pirrung M, Reeder J, Sevinsky JR, Turnbaugh PJ, Walters WA, Widmann J, Yatsunenko T, Zaneveld J, Knight R. QIIME allows analysis of high-throughput community sequencing data. Nat Methods. 2010;7:335–336. doi: 10.1038/nmeth.f.303.
    1. Richter M, Rosselló-Móra R. Shifting the genomic gold standard for the prokaryotic species definition. Proc Natl Acad Sci U S A. 2009;106:19126–19131. doi: 10.1073/pnas.0906412106.
    1. Kim M, Oh HS, Park SC, Chun J. Towards a taxonomic coherence between average nucleotide identity and 16S rRNA gene sequence similarity for species demarcation of prokaryotes. Int J Syst Evol Microbiol. 2014;64:346–351. doi: 10.1099/ijs.0.059774-0.
    1. Kim SW, Suda W, Kim S, Oshima K, Fukuda S, Ohno H, Morita H, Hattori M. Robustness of gut microbiota of healthy adults in response to probiotic intervention revealed by high-throughput pyrosequencing. DNA Res. 2013;20:241–253. doi: 10.1093/dnares/dst006.
    1. Subramanian S, Huq S, Yatsunenko T, Haque R, Mahfuz M, Alam MA, Benezra A, DeStefano J, Meier MF, Muegge BD, Barratt MJ, VanArendonk LG, Zhang Q, Province MA, Petri WA, Jr, Ahmed T, Gordon JI. Persistent gut microbiota immaturity in malnourished Bangladeshi children. Nature. 2014;510:417–421.
    1. Hartmann M, Howes CG, Abarenkov K, Mohn WW, Nilsson RH. V-Xtractor: an open-source, high-throughput software tool to identify and extract hypervariable regions of small subunit (16S/18S) ribosomal RNA gene sequences. J Microbiol Methods. 2010;83:250–253. doi: 10.1016/j.mimet.2010.08.008.
    1. Lozupone C, Knight R. UniFrac: a new phylogenetic method for comparing microbial communities. Appl Environ Microbiol. 2005;71:8228–8235. doi: 10.1128/AEM.71.12.8228-8235.2005.
    1. Hamady M, Lozupone C, Knight R. Fast UniFrac: facilitating high-throughput phylogenetic analyses of microbial communities including analysis of pyrosequencing and PhyloChip data. ISME J. 2010;4:17–27. doi: 10.1038/ismej.2009.97.
    1. Verhoeven KJF, Simonsen KL, McIntyre LM. Implementing false discovery rate control: increasing your power. Oikos. 2005;108:643–647. doi: 10.1111/j.0030-1299.2005.13727.x.
    1. R Development Core Team: R . A Language and Environment for Statistical Computing. Vienna, Austria: R Foundation for Statistical Computing; 2012.
    1. Grime JP. Benefits of plant diversity to ecosystems: immediate, filter and founder effects. J Ecol. 1998;86:902–910. doi: 10.1046/j.1365-2745.1998.00306.x.
    1. Kostic AD, Gevers D, Pedamallu CS, Michaud M, Duke F, Earl AM, Ojesina AI, Jung J, Bass AJ, Tabernero J, Baselga J, Liu C, Shivdasani RA, Ogino S, Birren BW, Huttenhower C, Garrett WS, Meyerson M. Genomic analysis identifies association of Fusobacterium with colorectal carcinoma. Genome Res. 2012;22:292–298. doi: 10.1101/gr.126573.111.
    1. Garrett WS, Gallini CA, Yatsunenko T, Michaud M, DuBois A, Delaney ML, Punit S, Karlsson M, Bry L, Glickman JN, Gordon JI, Onderdonk AB, Glimcher LH. Enterobacteriaceae act in concert with the gut microbiota to induce spontaneous and maternally transmitted colitis. Cell Host Microbe. 2010;8:292–300. doi: 10.1016/j.chom.2010.08.004.
    1. Bibiloni R, Schiffrin EJ. Intestinal host-microbe interactions under physiological and pathological conditions. Int J Inflamm. 2010;2010:386956. doi: 10.4061/2010/386956.
    1. Hu B, Elinav E, Huber S, Strowig T, Hao L, Hafemann A, Jin C, Eisenbarth SC, Flavell RA. Microbiota-induced activation of epithelial IL-6 signaling links inflammasome-driven inflammation with transmissible cancer. Proc Natl Acad Sci U S A. 2013;110:9862–9867. doi: 10.1073/pnas.1307575110.
    1. Ridaura VK, Faith JJ, Rey FE, Cheng J, Duncan AE, Kau AL, Griffin NW, Lombard V, Henrissat B, Bain JR, Muehlbauer MJ, Ilkayeva O, Semenkovich CF, Funai K, Hayashi DK, Lyle BJ, Martini MC, Ursell LK, Clemente JC, Van Treuren W, Walters WA, Knight R, Newgard CB, Heath AC, Gordon JI. Gut microbiota from twins discordant for obesity modulate metabolism in mice. Science. 2013;341:1241214. doi: 10.1126/science.1241214.
    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:e7125. doi: 10.1371/journal.pone.0007125.
    1. Santacruz A, Collado MC, Garcia-Valdes L, Segura MT, Martin-Lagos JA, Anjos T, Marti-Romero M, Lopez RM, Florido J, Campoy C, Sanz Y. Gut microbiota composition is associated with body weight, weight gain and biochemical parameters in pregnant women. Br J Nutr. 2010;104:83–92. doi: 10.1017/S0007114510000176.
    1. Zupancic ML, Cantarel BL, Liu Z, Drabek EF, Ryan KA, Cirimotich S, Jones C, Knight R, Walters WA, Knights D, Mongodin EF, Horenstein RB, Mitchell BD, Steinle N, Snitker S, Shuldiner AR, Fraser CM. Analysis of the gut microbiota in the old order Amish and its relation to the metabolic syndrome. PLoS One. 2012;7:e43052. doi: 10.1371/journal.pone.0043052.
    1. Kim DW, Shim JE, Paik HY, Song WO, Joung H. Nutritional intake of Korean population before and after adjusting for within-individual variations: 2001 Korean National Health and Nutrition Survey Data. Nutr Res Pract. 2011;5:266–274. doi: 10.4162/nrp.2011.5.3.266.
    1. National Institute of Health and Nutrition: Outline for the Results of the National Health and Nutrition Survey Japan, 2007. []
    1. What We Eat In America, NHANES 2009–2010: Documentation and Data Files []
    1. Elmadfa I (volume editor) European Nutrition and Health Report 2009. Vienna (Austria): European Commission, Health and Consumer Protection, Directorate-General; 2009.
    1. Yoonna L, Hae-Jeung L, Haeng-Shin L, Young-Ai J, Cho-il K. Analytical dietary fiber database for the National Health and Nutrition Survey in Korea. J Food Composition Anal. 2008;21:S35–S42. doi: 10.1016/j.jfca.2007.07.008.
    1. McDonald D, Price MN, Goodrich J, Nawrocki EP, DeSantis TZ, Probst A, Andersen GL, Knight R, Hugenholtz P. An improved Greengenes taxonomy with explicit ranks for ecological and evolutionary analyses of bacteria and archaea. ISME J. 2012;6:610–618. doi: 10.1038/ismej.2011.139.
    1. Bahl MI, Bergstrom A, Licht TR. Freezing fecal samples prior to DNA extraction affects the Firmicutes to Bacteroidetes ratio determined by downstream quantitative PCR analysis. FEMS Microbiol Lett. 2012;329:193–197. doi: 10.1111/j.1574-6968.2012.02523.x.
    1. Hildebrandt MA, Hoffmann C, Sherrill-Mix SA, Keilbaugh SA, Hamady M, Chen YY, Knight R, Ahima RS, Bushman F, Wu GD. High-fat diet determines the composition of the murine gut microbiome independently of obesity. Gastroenterology. 2009;137:1716–1724. doi: 10.1053/j.gastro.2009.08.042.
    1. Mozes S, Bujnakova D, Sefcikova Z, Kmet V. Developmental changes of gut microflora and enzyme activity in rat pups exposed to fat-rich diet. Obesity. 2008;16:2610–2615. doi: 10.1038/oby.2008.435.
    1. Guo X, Xia X, Tang R, Zhou J, Zhao H, Wang K. Development of a real-time PCR method for Firmicutes and Bacteroidetes in faeces and its application to quantify intestinal population of obese and lean pigs. Lett Appl Microbiol. 2008;47:367–373. doi: 10.1111/j.1472-765X.2008.02408.x.
    1. Everard A, Belzer C, Geurts L, Ouwerkerk JP, Druart C, Bindels LB, Guiot Y, Derrien M, Muccioli GG, Delzenne NM, Schrenze J, Cani PD. Cross-talk between Akkermansia muciniphila and intestinal epithelium controls diet-induced obesity. Proc Natl Acad Sci U S A. 2013;110:9066–9071. doi: 10.1073/pnas.1219451110.
    1. Million M, Thuny F, Angelakis E, Casalta JP, Giorgi R, Habib G, Raoult D. Lactobacillus reuteri and Escherichia coli in the human gut microbiota may predict weight gain associated with vancomycin treatment. Nutrition & Diabetes. 2013;3:e87. doi: 10.1038/nutd.2013.28.
    1. Bhatt AS, Freeman SS, Herrera AF, Pedamallu CS, Gevers D, Duke F, Jung J, Michaud M, Walker BJ, Young S, Earl AM, Kostic AD, Ojesina AI, Hasserjian R, Ballen KK, Chen YB, Hobbs G, Antin JH, Soiffer RJ, Baden LR, Garrett WS, Hornick JL, Marty FM, Meyerson M. Sequence-based discovery of Bradyrhizobium enterica in cord colitis syndrome. N Engl J Med. 2013;369:517–528. doi: 10.1056/NEJMoa1211115.
    1. Raman M, Ahmed I, Gillevet PM, Probert CS, Ratcliffe NM, Smith S, Greenwood R, Sikaroodi M, Lam V, Crotty P, Bailey J, Myers RP, Rioux KP. Fecal microbiome and volatile organic compound metabolome in obese humans with nonalcoholic fatty liver disease. Clin Gastroenterol Hepatol. 2013;11:868–875. doi: 10.1016/j.cgh.2013.02.015.
    1. Wong VW, Tse CH, Lam TT, Wong GL, Chim AM, Chu WC, Yeung DK, Law PT, Kwan HS, Yu J, Sung JJ, Chan HL. Molecular characterization of the fecal microbiota in patients with nonalcoholic steatohepatitis–a longitudinal study. PLoS One. 2013;8:e62885. doi: 10.1371/journal.pone.0062885.
    1. Chen W, Liu F, Ling Z, Tong X, Xiang C. Human intestinal lumen and mucosa-associated microbiota in patients with colorectal cancer. PLoS One. 2012;7:e39743. doi: 10.1371/journal.pone.0039743.
    1. van Passel MW, Kant R, Zoetendal EG, Plugge CM, Derrien M, Malfatti SA, Chain PS, Woyke T, Palva A, de Vos WM, Smidt H. The genome of Akkermansia muciniphila, a dedicated intestinal mucin degrader, and its use in exploring intestinal metagenomes. PLoS One. 2011;6:e16876. doi: 10.1371/journal.pone.0016876.
    1. Axling U, Olsson C, Xu J, Fernandez C, Larsson S, Strom K, Ahrne S, Holm C, Molin G, Berger K. Green tea powder and Lactobacillus plantarum affect gut microbiota, lipid metabolism and inflammation in high-fat fed C57BL/6 J mice. Nutr Metab. 2012;9:105. doi: 10.1186/1743-7075-9-105.
    1. Karlsson CLJ, Onnerfalt J, Xu J, Molin G, Ahrne S, Thorngren-Jerneck K. The microbiota of the gut in preschool children with normal and excessive body weight. Obesity. 2012;20:2257–2261. doi: 10.1038/oby.2012.110.
    1. Shin NR, Lee JC, Lee HY, Kim MS, Whon TW, Lee MS, Bae JW. An increase in the Akkermansia spp. population induced by metformin treatment improves glucose homeostasis in diet-induced obese mice. Gut. 2013;63:727–735. doi: 10.1136/gutjnl-2012-303839.

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