Faecal microbiota composition in adults is associated with the FUT2 gene determining the secretor status

PLoS ONE

Volumn 9, Issue 4, 2014, Pages

  Wacklin, Pirjo ^a   Tuimala, Jarno ^a   Nikkilä, Janne ^a   Tims, Sebastian ^d   Mäkivuokko, Harri ^a   Alakulppi, Noora ^a   Laine, Pia ^b   Rajilic Stojanovic, Mirjana ^d   Paulin, Lars ^b   De Vos, Willem M ^c,d   Mättö, Jaana ^a  

^a FINNISH RED CROSS BLOOD SERVICE   (Finland)

^b UNIVERSITY OF HELSINKI   (Finland)

^c UNIVERSITY OF HELSINKI   (Finland)

^d WAGENINGEN UNIVERSITY   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

FUCOSYLTRANSFERASE; FUCOSYLTRANSFERASE 2; RNA 16S; UNCLASSIFIED DRUG; GALACTOSIDE 2-ALPHA-L-FUCOSYLTRANSFERASE;

16S RRNA GENE; ADULT; ARTICLE; BLOOD GROUP ABO SYSTEM; BLOOD GROUP LEWIS SYSTEM; BLOOD GROUP SYSTEM; CONTROLLED STUDY; DENATURING GRADIENT GEL ELECTROPHORESIS; ETHNIC GROUP; FECES MICROFLORA; FUCOSYLTRANSFERASE 2 GENE; GENETIC ANALYSIS; GENETIC ASSOCIATION; GENETIC POLYMORPHISM; GENOTYPE; HUMAN; INTESTINE FLORA; INTESTINE MUCOSA; MICROARRAY ANALYSIS; NONHUMAN; PHYLOGENY; POLYMERASE CHAIN REACTION; PYROSEQUENCING; SECRETOR STATUS; SPECIES RICHNESS; WESTERN EUROPEAN; DNA MICROARRAY; DNA SEQUENCE; FECES; GENETICS; MICROBIOLOGY; MICROFLORA; SECRETION (PROCESS);

ADULT; DENATURING GRADIENT GEL ELECTROPHORESIS; FECES; FUCOSYLTRANSFERASES; HUMANS; MICROBIOTA; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PHYLOGENY; SEQUENCE ANALYSIS, DNA;

EID: 84899648332     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0094863     Document Type: Article

References (59)

1. Rajilic-Stojanovic M, Heilig HG, Tims S, Zoetendal EG, de Vos WM (2013). Long-term monitoring of the human intestinal microbiota composition. Environ Microbiol 15: 1146-1159.
2. Zoetendal EG, Akkermans ADL, Akkermans-van Vliet WM, de Visser, J. Arjan G M., et al. (2001). The Host Genotype Affects the Bacterial Community in the Human Gastronintestinal Tract. Microbial Ecology in Health and Disease 13: 129-134.
3. Tims S, Derom C, Jonkers DM, Vlietinck R, Saris WH, et al. (2013). Microbiota conservation and BMI signatures in adult monozygotic twins. ISME J 7: 707-717.
4. Turnbaugh PJ, Hamady M, Yatsunenko T, Cantarel BL, Duncan A, et al. (2009). A core gut microbiome in obese and lean twins. Nature 457: 480-484.
5. Yatsunenko T, Rey FE, Manary MJ, Trehan I, Dominguez-Bello MG, et al. (2012). Human gut microbiome viewed across age and geography. Nature 486: 222-227.
6. de Vos WM, de Vos EA (2012). Role of the intestinal microbiome in health and disease: from correlation to causation. Nutr Rev 70: S45-56.
7. Wacklin P, Mäkivuokko H, Alakulppi N, Nikkilä J, Tenkanen H, et al. (2011). Secretor genotype (FUT2 gene) is strongly associated with the composition of Bifidobacteria in the human intestine. PLoS One 6: e20113.
8. Kashyap PC, Marcobal A, Ursell LK, Smits SA, Sonnenburg ED, et al. (2013). Genetically dictated change in host mucus carbohydrate landscape exerts a dietdependent effect on the gut microbiota. Proc Natl Acad Sci U S A 110: 17059-17064.
9. McGovern DP, Jones MR, Taylor KD, Marciante K, Yan X, et al. (2010). Fucosyltransferase 2 (FUT2) non-secretor status is associated with Crohn's disease. Hum Mol Genet 19: 3468-3476.
10. Smyth DJ, Cooper JD, Howson JM, Clarke P, Downes K, et al. (2011). FUT2 nonsecretor status links type 1 diabetes susceptibility and resistance to infection. Diabetes 60: 3081-3084.
11. Hurd EA, Domino SE (2004). Increased susceptibility of secretor factor gene Fut2-null mice to experimental vaginal candidiasis. Infect Immun 72: 4279-4281.
12. Sheinfeld J, Schaeffer AJ, Cordon-Cardo C, Rogatko A, et al. (1989). Association of the Lewis blood-group phenotype with recurrent urinary tract infections in women. N Engl J Med 320: 773-777.
13. Ng KM, Ferreyra JA, Higginbottom SK, Lynch JB, Kashyap PC, et al.(2013) Microbiota-liberated host sugars facilitate post-antibiotic expansion of enteric pathogens. Nature 502: 96-99.
14. Rausch P, Rehman A, Kunzel S, Hasler R, Ott SJ, et al. (2011). Colonic mucosa-associated microbiota is influenced by an interaction of Crohn disease and FUT2 (Secretor) genotype. Proc Natl Acad Sci U S A 108: 19030-19035.
15. Belzer C, de Vos WM (2012). Microbes inside-from diversity to function: the case of Akkermansia. ISME J 6: 1449-1458.
16. Arumugam M, Raes J, Pelletier E, Le Paslier D, Yamada T, et al. (2011). Enterotypes of the human gut microbiome. Nature 473: 174-180.
17. Huse SM, Ye Y, Zhou Y, Fodor AA (2012). A core human microbiome as viewed through 16S rRNA sequence clusters. PLoS One 7: e34242.
18. Koren O, Knights D, Gonzalez A, Waldron L, Segata N, et al. (2013). A Guide to enterotypes across the human body: Meta-analysis of microbial community structures in human microbiome datasets. PLoS Comput Biol 9: e1002863.
19. Wu GD, Chen J, Hoffmann C, Bittinger K, Chen YY, et al. (2011). Linking long-term dietary patterns with gut microbial enterotypes. Science 334: 105-108.
20. Quince C, Lundin EE, Andreasson AN, Greco D, Rafter J, et al. (2013). The impact of Crohn's disease genes on healthy human gut microbiota: a pilot study. Proc Natl Acad Sci U S A 110: 654-659.
21. Miyoshi J, Yajima T, Okamoto S, Matsuoka K, Inoue N, et al. (2011). Ectopic expression of blood type antigens in inflamed mucosa with higher incidence of FUT2 secretor status in colonic Crohn's disease. J Gastroenterol 46: 1056-1063.
22. Rajilic-Stojanovic M (2007). Diversity of human gastrointestinal microbiota. Novel perspestives from high throughput analyses. Wageningen: Wageningen University and Research Centre. 214 p.
23. Rajilic-Stojanovic M, Biagi E, Heilig HG, Kajander K, Kekkonen RA, et al. (2011). Global and deep molecular analysis of microbiota signatures in fecal samples from patients with irritable bowel syndrome. Gastroenterology 141: 1792-1801.
24. Willing BP, Dicksved J, Halfvarson J, Andersson AF, Lucio M, et al. (2010). A pyrosequencing study in twins shows that gastrointestinal microbial profiles vary with inflammatory bowel disease phenotypes. Gastroenterology 139: 1844-1854.
25. Sanz Y, De Pama G, Laparra M (2011). Unraveling the ties between celiac disease and intestinal microbiota. Int Rev Immunol 30: 207-218.
26. Wen L, Ley RE, Volchkov PY, Stranges PB, Avanesyan L, et al. (2008). Innate immunity and intestinal microbiota in the development of Type 1 diabetes. Nature 455: 1109-1113.
27. Parmar AS, Alakulppi N, Paavola-Sakki P, Kurppa K, Halme L, et al. (2012). Association study of FUT2 (rs601338) with celiac disease and inflammatory bowel disease in the Finnish population. Tissue Antigens 80: 488-493.
28. Koropatkin NM, Cameron EA, Martens EC (2012). How glycan metabolism shapes the human gut microbiota. Nat Rev Microbiol 10: 323-335.
29. Marcobal A, Barboza M, Sonnenburg ED, Pudlo N, Martens EC, et al. (2011). Bacteroides in the infant gut consume milk oligosaccharides via mucusutilization pathways. Cell Host Microbe 10: 507-514.
30. Anderson KM, Ashida H, Maskos K, Dell A, Li SC, Li YT (2005). A clostridial endo-beta-galactosidase that cleaves both blood group A and B glycotopes: the first member of a new glycoside hydrolase family, GH98. J Biol Chem 280: 7720-7728.
31. Hata DJ, Smith DS (2004). Blood group B degrading activity of Ruminococcus gnavus alpha-galactosidase. Artif Cells Blood Substit Immobil Biotechnol 32: 263-274.
32. Henry S, Oriol R, Samuelsson B (1995). Lewis histo-blood group system and associated secretory phenotypes. Vox Sang 69: 166-182.
33. Hoskins LC, Boulding ET (1976). Degradation of blood group antigens in human colon ecosystems. I. In vitro production of ABH blood group-degrading enzymes by enteric bacteria. J Clin Invest 57: 63-73.
34. Katayama T, Sakuma A, Kimura T, Makimura Y, Hiratake J, et al. (2004). Molecular cloning and characterization of Bifidobacterium bifidum 1,2-alpha-Lfucosidase (AfcA), a novel inverting glycosidase (glycoside hydrolase family 95). J Bacteriol 186: 4885-4893.
35. van Passel MW, Kant R, Zoetendal EG, Plugge CM, Derrien M, et al. (2011). The genome of Akkermansia muciniphila, a dedicated intestinal mucin degrader, and its use in exploring intestinal metagenomes. PLoS One 6: e16876.
36. Stewart CS, Duncan SH, Cave DR (2004). Oxalobacter formigenes and its role in oxalate metabolism in the human gut. FEMS Microbiol Lett 230: 1-7.
37. Boren T, Falk P, Roth KA, Larson G, Normark S (1993). Attachment of Helicobacter pylori to human gastric epithelium mediated by blood group antigens. Science 262: 1892-1895.
38. Nurjadi D, Lependu J, Kremsner PG, Zanger P (2012). Staphylococcus aureus throat carriage is associated with ABO-/secretor status. J Infect 65: 310-317.
39. Uchida H, Kinoshita H, Kawai Y, Kitazawa H, Miura K, et al. (2006). Lactobacilli binding human A-antigen expressed in intestinal mucosa. Res Microbiol 157: 659-665.
40. Rehman A, Sina C, Gavrilova O, Hä sler R, Ott S, et al. (2011). Nod2 is essential for temporal development of intestinal microbial communities. Gut 2011 60: 1354-62
41. Spor A, Koren O, Ley R (2011). Unravelling the effects of the environment and host genotype on the gut microbiome. Nat Rev Microbiol 9: 279-290.
42. Claesson, O'Sullivan O, Wang Q, Nikkilä J, Marchesi JR, et al. (2009). Comparative Analysis of Pyrosequencing and a Phylogenetic Microarray for Exploring Microbial Community Structures in the Human Distal Intestine. PLoS ONE 4(8): e6669.
43. 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.
44. Apajalahti JH, Sä rkilahti LK, Mäki BR, Heikkinen JP, Nurminen PH, et al. (1998). Effective recovery of bacterial DNA and percent-guanine-plus- cytosinebased analysis of community structure in the gastrointestinal tract of broiler chickens. Appl Environ Microbiol 64: 4084-4088.
45. Mäkivuokko H, Lahtinen SJ, Wacklin P, Tuovinen E, Tenkanen H, et al. (2012). Association between the ABO blood group and the human intestinal microbiota composition. BMC Microbiol 12: 94.
46. Oksanen J, Blanchet FG, Kindt R, Legendre P, O'Hara RB, et al. (2012). Vegan: Community Ecology Package. R package, version 2.0-3.
47. Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, et al. (2009). Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75: 7537-7541.
48. Pruesse E, Quast,C, Knittel K, Fuchs BM, Ludwig W, et al. (2007). SILVA: a comprehensive online resource for quality checked and aligned ribosomal RNA sequence data compatible with ARB Nucl Acids Res 35: 7188-7196.
49. Rossi J (2011). Rich: Species richness estimation and comparison. R package version 0.1.
50. Manly BFJ (1997). Randomization and Monte Carlo methods in biology. London: Chapman & Hall. 399 p.
51. Dufrene M, Legendre P (1997). Species Assemblages and Indicator Species: The Need for a Flexible Asymmetrical Approach. Ecol Monogr 67: 345-366.
52. Roberts DW (2010). Labdsv: Ordination and Multivariate Analysis for Ecology. R package version 1.4-1.
53. Legendre P, Gallagher E (2001). Ecologically meaningful transformations for ordination of species data. Oecologia 129: 271-280.
54. Excoffier L, Smouse PE, Quattro JM (1992). Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 131: 479-491.
55. Paradis E (2010). Pegas: an R package for population genetics with an integrated-modular approach. Bioinformatics 26: 419-420.
56. Rajilic-Stojanovic M, Heilig HG, Molenaar D, Kajander K, Surakka A, 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.
57. Bolstad BM, Irizarry RA, Astrand M, Speed TP (2003). A comparison of normalization methods for high density oligonucleotide array data based on variance and bias. Bioinformatics 19: 185-193.
58. Breiman L (2001). Random Forests. Mach Learn 45: 5-32.
59. Bastian M, Heymann S, Jacomy M (2009). Gephi: an open source software for exploring and manipulating networks. International AAAI Conference on Weblogs and Social Media. Available: https://gephi.org/users/publications/.