Microbiota conservation and BMI signatures in adult monozygotic twins

ISME Journal

Volumn 7, Issue 4, 2013, Pages 707-717

  Tims, Sebastian ^a   Derom, Catherine ^b   Jonkers, Daisy M ^c   Vlietinck, Robert ^b   Saris, Wim H ^c   Kleerebezem, Michiel ^a,d   De Vos, Willem M ^a,e   Zoetendal, Erwin G ^a  

^a TOP INSTITUTE FOOD AND NUTRITION   (Netherlands)

^b UNIVERSITY HOSPITALS LEUVEN   (Belgium)

^c MAASTRICHT UNIVERSITY MEDICAL CENTER   (Netherlands)

^d NIZO FOOD RESEARCH   (Netherlands)

^e UNIVERSITY OF HELSINKI   (Finland)

Author keywords

BMI signatures; discordant BMI; gastrointestinal tract; microbiota; monozygotic twins

Indexed keywords

BACTERIAL DNA; RNA 16S;

ADULT; BACTERIUM; BODY MASS; ENERGY BALANCE; FERMENTATION; GENOTYPE; HOMEOSTASIS; MICROBIAL ACTIVITY; MICROORGANISM; PHYLOGENETICS;

ADULT; ARTICLE; BODY MASS; CLASSIFICATION; DIETARY FIBER; ENDOSPORE-FORMING RODS AND COCCI; FECES; GASTROINTESTINAL TRACT; GENETICS; HUMAN; ISOLATION AND PURIFICATION; METABOLISM; METAGENOME; MICROBIOLOGY; MONOZYGOTIC TWINS; PHYLOGENY; TWINS;

ADULT; BODY MASS INDEX; DIETARY FIBER; DNA, BACTERIAL; FECES; GASTROINTESTINAL TRACT; GRAM-POSITIVE ENDOSPORE-FORMING RODS; HUMANS; METAGENOME; PHYLOGENY; RNA, RIBOSOMAL, 16S; TWINS, MONOZYGOTIC;

CLOSTRIDIUM; EUBACTERIUM VENTRIOSUM; OSCILLOSPIRA GUILLIERMONDII; ROSEBURIA INTESTINALIS;

EID: 84875370244     PISSN: 17517362     EISSN: 17517370     Source Type: Journal    
DOI: 10.1038/ismej.2012.146     Document Type: Article

References (67)

1. Adlercreutz H, Pulkkinen MO, Hämäläinen EK, Korpela JT. (1984). Studies on the role of intestinal bacteria in metabolism of synthetic and natural steroid hormones. J Steroid Biochem 20: 217-229.
2. Albert MJ, Mathan VI, Baker SJ. (1980). Vitamin B12 synthesis by human small intestinal bacteria. Nature 283: 781-782.
3. Amos HE, Little CO, Mitchell GE Jr. (1971). Proline utilization during cellulose fermentation by rumen microorganisms. J Agric Food Chem 19: 112-115.
4. Arumugam M, Raes J, Pelletier E, Le Paslier D, Yamada T, Mende DR et al. (2011). Enterotypes of the human gut microbiome. Nature 473: 174-180.
5. Backhed F, Ding H, Wang T, Hooper LV, Koh GY, Nagy A et al. (2004). The gut microbiota as an environmental factor that regulates fat storage. Proc Natl Acad Sci USA 101: 15718-15723.
6. Backhed F, Manchester JK, Semenkovich CF, Gordon JI. (2007). Mechanisms underlying the resistance to dietinduced obesity in germ-free mice. Proc Natl Acad Sci USA 104: 979-984.
7. Barcenilla A, Pryde SE, Martin JC, Duncan SH, Stewart CS, Henderson C et al. (2000). Phylogenetic relationships of butyrate-producing bacteria from the human gut. Appl Environ Microbiol 66: 1654-1661.
8. Begley M, Gahan CG, Hill C. (2005). The interaction between bacteria and bile. FEMS Microbiol Rev 29: 625-651.
9. Benson AK, Kelly SA, Legge R, Ma F, Low SJ, Kim J et al. (2010). Individuality in gut microbiota composition is a complex polygenic trait shaped by multiple environmental and host genetic factors. Proc Natl Acad Sci USA 107: 18933-18938.
10. Booijink CC, Zoetendal EG, Kleerebezem M, de Vos WM. (2007). Microbial communities in the human small intestine: coupling diversity to metagenomics. Future Microbiol 2: 285-295.
11. Bouchard C, Tremblay A, Després JP, Nadeau A, Lupien PJ, Thériault G et al. (1990). The response to long-term overfeeding in identical twins. N Engl J Med 322: 1477-1482.
12. Cebra JJ. (1999). Influences of microbiota on intestinal immune system development. Am J Clin Nutr 69: 1046S-1051S.
13. Claesson MJ, Cusack S, O'Sullivan O, Greene-Diniz R, de Weerd H, Flannery E et al. (2011). Composition, variability, and temporal stability of the intestinal microbiota of the elderly. Proc Natl Acad Sci USA 108(Suppl 1): 4586-4591.
14. Claesson MJ, O'Sullivan O, Wang Q, Nikkilä J, Marchesi JR, Smidt H et al. (2009). Comparative analysis of pyrosequencing and a phylogenetic microarray for exploring microbial community structures in the human distal intestine. PLoS One 4: e6669.
15. Cummings JH, Macfarlane GT. (1997). Colonic microflora: nutrition and health. Nutrition 13: 476-478.
16. Derom CA, Vlietinck RF, Thiery EW, Leroy FO, Fryns JP, Derom RM. (2006). The East Flanders Prospective Twin Survey (EFPTS). Twin Res Hum Genet 9: 733-738.
17. Dicksved J, Halfvarson J, Rosenquist M, Järnerot G, Tysk C, Apajalahti J et al. (2008). Molecular analysis of the gut microbiota of identical twins with crohn's disease. ISME J 2: 716-727.
18. Duncan SH, Hold GL, Barcenilla A, Stewart CS, Flint HJ. (2002). Roseburia intestinalis sp. nov., a novel saccharolytic, butyrate-producing bacterium from human faeces. Int J Syst Evol Microbiol 52(Part 5): 1615-1620.
19. Duncan SH, Lobley GE, Holtrop G, Ince J, Johnstone AM, Louis P et al. (2008). Human colonic microbiota associated with diet, obesity and weight loss. Int J Obes (Lond) 32: 1720-1724.
20. Grech-Mora I et al. (1996). Isolation and characterization of sporobacter termitidis gen. nov., sp. nov., from the digestive tract of the wood-feeding termite nasutitermes lujae. Int J Syst Bacteriol 46: 512-518.
21. Hamady M, Knight R. (2009). Microbial community profiling for human microbiome projects: tools, techniques, and challenges. Genome Res 19: 1141-1152.
22. Heid IM, Jackson AU, Randall JC, Winkler TW, Qi L, Steinthorsdottir V et al. (2011). Meta-analysis identifies 13 new loci associated with waist-hip ratio and reveals sexual dimorphism in the genetic basis of fat distribution 43: 1164-1164.
23. Huse SM, Ye Y, Zhou Y, Fodor AA. (2012). A core human microbiome as viewed through 16S rRNA sequence clusters. PLoS One 7: e34242.
24. Jalanka-Tuovinen J, Salonen A, Nikkilä J, Immonen O, Kekkonen R, Lahti L et al. (2011). Intestinal microbiota in healthy adults: temporal analysis reveals individual and common core and relation to intestinal symptoms. PLoS One 6: e23035.
25. Klieve AV, O'Leary MN, McMillen L, Ouwerkerk D. (2007). Ruminococcus bromii, identification and isolation as a dominant community member in the rumen of cattle fed a barley diet. J Appl Microbiol 103: 2065-2073.
26. Kovatcheva-Datchary P, Egert M, Maathuis A, Rajilić- Stojanović M, de Graaf AA, Smidt H et al. (2009). Linking phylogenetic identities of bacteria to starch fermentation in an in vitro model of the large intestine by RNA-based stable isotope probing. Environ Microbiol 11: 914-926.
27. Lepage P, Häsler R, Spehlmann ME, Rehman A, Zvirbliene A, Begun A et al. (2011). Twin study indicates loss of interaction between microbiota and mucosa of patients with ulcerative colitis. Gastroenterology 141: 227-236.
28. Ley RE, khed F, Turnbaugh P, Lozupone CA, Knight RD, Gordon JI. (2005). Obesity alters gut microbial ecology. Proc Natl Acad Sci USA 102: 11070-11075.
29. Ley RE, Turnbaugh PJ, Klein S, Gordon JI. (2006). Microbial ecology: human gut microbes associated with obesity. Nature 444: 1022-1023.
30. Mackie RI, Aminov RI, Hu W, Klieve AV, Ouwerkerk D, Sundset MA et al. (2003). Ecology of uncultivated Oscillospira species in the rumen of cattle, sheep, and reindeer as assessed by microscopy and molecular approaches. Appl Environ Microbiol 69: 6808-6815.
31. Manichanh C, Rigottier-Gois L, Bonnaud E, Gloux K, Pelletier E, Frangeul L et al. (2006). Reduced diversity of faecal microbiota in Crohn's disease revealed by a metagenomic approach. Gut 55: 205-211.
32. Manson JE, Willett WC, Stampfer MJ, Colditz GA, Hunter DJ, Hankinson SE et al. (1995). Body weight and mortality among women. N Engl J Med 333: 677-685.
33. Matthies C, Evers S, Ludwig W, Schink B. (2000). Anaerovorax odorimutans gen. nov., sp. nov., a putrescine-fermenting, strictly anaerobic bacterium. Int J Syst Evol Microbiol 50(Part 4): 1591-1594.
34. Metges CC. (2000). Contribution of microbial amino acids to amino acid homeostasis of the host. J Nutr 130: 1857S-1864S.
35. Naukkarinen J, Surakka I, Pietiläinen KH, Rissanen A, Salomaa V, Ripatti S et al. (2010). Use of genome-wide expression data to mine the 'Gray Zone' of GWA studies leads to novel candidate obesity genes. PloS Genet 6: e1000976.
36. O'Hara AM, O'Regan P, Fanning A, O'Mahony C, Macsharry J, Lyons A et al. (2006). Functional modulation of human intestinal epithelial cell responses by Bifidobacterium infantis and Lactobacillus salivarius. Immunology 118: 202-215.
37. Pietilainen KH, Naukkarinen J, Rissanen A, Saharinen J, Ellonen P, Keränen H et al. (2008). Global transcript profiles of fat in monozygotic twins discordant for BMI: pathways behind acquired obesity. Plos Med 5: e51.
38. Pryde SE, Duncan SH, Hold GL, Stewart CS, Flint HJ. (2002). The microbiology of butyrate formation in the human colon. FEMS Microbiol Lett 217: 133-139.
39. Qin J, Li R, Raes J, Arumugam M, Burgdorf KS, Manichanh C et al. (2010). A human gut microbial gene catalogue established by metagenomic sequencing. Nature 464: 59-65.
40. Rajilic-Stojanovic M, Heilig HG, Molenaar D, Kajander K, Surakka A, Smidt H et al. (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: 1736-1751.
41. Ramotar K, Conly JM, Chubb H, Louie TJ. (1984). Production of menaquinones by intestinal anaerobes. J Infect Dis 150: 213-218.
42. Salonen A, Nikkilä J, Jalanka-Tuovinen J, Immonen O, Rajilić-Stojanović M, Kekkonen RA et al. (2010). Comparative analysis of fecal DNA extraction methods with phylogenetic microarray: effective recovery of bacterial and archaeal DNA using mechanical cell lysis. J Microbiol Methods 81: 127-134.
43. Salonen A, Salojärvi J, Lahti L, de Vos WM. (2012). The adult intestinal core microbiota is determined by analysis depth and health status. Clin Microbiol Infect 18(Suppl 4): 16-20.
44. Samuel BS, Shaito A, Motoike T, Rey FE, Backhed F, Manchester JK et al. (2008). Effects of the gut microbiota on host adiposity are modulated by the short-chain fatty-acid binding G protein-coupled receptor, Gpr41. Proc Natl Acad Sci USA 105: 16767-16772.
45. Saris WH, Tarnopolsky MA. (2003). Controlling food intake and energy balance: which macronutrient should we select? Curr Opin Clin Nutr Metab Care 6: 609-613.
46. Savage DC. (1977). Microbial ecology of the gastrointestinal tract. Annu Rev Microbiol 31: 107-133.
47. Schwiertz A, Taras D, Schäfer K, Beijer S, Bos NA, Donus C et al. (2010). Microbiota and SCFA in lean and overweight healthy subjects. Obesity (Silver Spring) 18: 190-195.
48. Seksik P, Rigottier-Gois L, Gramet G, Sutren M, Pochart P, Marteau P et al. (2003). Alterations of the dominant faecal bacterial groups in patients with Crohn's disease of the colon. Gut 52: 237-242.
49. Shanahan F. (2002). The host-microbe interface within the gut. Best Pract Res Clin Gastroenterol 16: 915-931.
50. Stams AJ, Van Dijk JB, Dijkema C, Plugge CM. (1993). Growth of syntrophic propionate-oxidizing bacteria with fumarate in the absence of methanogenic bacteria. Appl Environ Microbiol 59: 1114-1119.
51. Stevens J, Truesdale KP, McClain JE, Cai J. (2006). The definition of weight maintenance. Int J Obes 30: 391-399.
52. Stevens J, Cai J, Pamuk ER, Williamson DF, Thun MJ, Wood JL. (1998). The effect of age on the association between body-mass index and mortality. N Engl J Med 338: 1-7.
53. Stewart JA, Chadwick VS, Murray A. (2005). Investigations into the influence of host genetics on the predominant eubacteria in the faecal microflora of children. J Med Microbiol 54: 1239-1242.
54. Tap J, Mondot S, Levenez F, Pelletier E, Caron C, Furet JP et al. (2009). Towards the human intestinal microbiota phylogenetic core. Environ Microbiol 11: 2574-2584.
55. Turnbaugh PJ, Hamady M, Yatsunenko T, Cantarel BL, Duncan A, Ley RE et al. (2009). A core gut microbiome in obese and lean twins. Nature 457: 480-484.
56. Turnbaugh PJ, Ley RE, Mahowald MA, Magrini V, Mardis ER, Gordon JI. (2006). An obesity-associated gut microbiome with increased capacity for energy harvest. Nature 444: 1027-1031.
57. Van de Merwe JP, Stegeman JH, Hazenberg MP. (1983). The resident faecal flora is determined by genetic characteristics of the host. Implications for Crohn's disease? Antonie Van Leeuwenhoek 49: 119-124.
58. van den Bogert B, de Vos WM, Zoetendal EG, Kleerebezem M. (2011). Microarray analysis and barcoded pyrosequencing provide consistent microbial profiles depending on the source of human intestinal samples. Appl Environ Microbiol 77: 2071-2080.
59. Visser M, Bouter LM, McQuillan GM, Wener MH, Harris TB. (1999). ELevated c-reactive protein levels in overweight and obese adults. JAMA 28222 2131-2135.
60. Wei C, Brent MR. (2006). Using ESTs to improve the accuracy of de novo gene prediction. BMC Bioinform 7: 327.
61. Willing BP, Dicksved J, Halfvarson J, Andersson AF, Lucio M, Zheng Z et al. (2010). A pyrosequencing study in twins shows that gastrointestinal microbial profiles vary with inflammatory bowel disease phenotypes. Gastroenterology 139: 1844-1854.
62. Wu GD, Chen J, Hoffmann C, Bittinger K, Chen YY, Keilbaugh SA et al. (2011). Linking long-term dietary patterns with gut microbial enterotypes. Science 334: 105-108.
63. Yang X, Xie L, Li Y, Wei C. (2009). More than 9,000,000 unique genes in human gut bacterial community: estimating gene numbers inside a human body. PLoS One 4: e6074.
64. Yanling H, Youfang D, Yanquan L. (1991). Two cellulolytic clostridium species: clostridium cellulosi sp. nov. and clostridium cellulofermentans sp. nov. Int J Syst Bacteriol 41: 306-309.
65. Zhang H, DiBaise JK, Zuccolo A, Kudrna D, Braidotti M, Yu Y et al. (2009). Human gut microbiota in obesity and after gastric bypass. Proc Natl Acad Sci USA 106: 2365-2370.
66. Zoetendal EG et al. (2001). The host genotype affects the bacterial community in the human gastronintestinal tract. Microb Ecol Health Dis 13: 129-134.
67. Zoetendal EG, Cheng B, Koike S, Mackie RI. (2004). Molecular microbial ecology of the gastrointestinal tract: from phylogeny to function. Curr Issues Intest Microbiol 5: 31-47.