FUT2 genotype and secretory status are not associated with fecal microbial composition and inferred function in healthy subjects

Gut Microbes

Volumn 9, Issue 4, 2018, Pages 357-368

  Turpin, Williams ^a,b   Bedrani, Larbi ^a,b   Espin Garcia, Osvaldo ^c,d   Xu, Wei ^d   Silverberg, Mark S ^a   Smith, Michelle I ^a,b   Guttman, David S ^d,e   Griffiths, Anne ^f   Moayyedi, Paul ^g   Panaccione, Remo ^h   Huynh, Hien ⁱ   Steinhart, Hillary ^a,b   Aumais, Guy ^j   Shestopaloff, Konstantin ^d   Dieleman, Levinus A ⁱ   Turner, Dan ^k   Paterson, Andrew D ^d,l   Croitoru, Kenneth ^a,b  

^a MOUNT SINAI HOSPITAL   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

^c MOUNT SINAI HOSPITAL   (Canada)

^d UNIVERSITY OF TORONTO   (Canada)

^e UNIVERSITY OF TORONTO   (Canada)

^f HOSPITAL FOR SICK CHILDREN   (Canada)

^g MCMASTER UNIVERSITY   (Canada)

^h UNIVERSITY OF CALGARY   (Canada)

ⁱ UNIVERSITY OF ALBERTA   (Canada)

^j MAISONNEUVE ROSEMONT HOSPITAL   (Canada)

^k SHAARE ZEDEK MEDICAL CENTER   (Israel)

^l HOSPITAL FOR SICK CHILDREN RESEARCH INSTITUTE   (Canada)

more..

Author keywords

ABO antigen; Blood group antigens; Fecal microbiota; Fucosylation; Gut microbiota; Healthy human; human genetic; Microbiome; mucus

Indexed keywords

BLOOD GROUP H ANTIGEN; FUCOSE; FUCOSYLTRANSFERASE; FUCOSYLTRANSFERASE 2; GENOMIC DNA; RNA 16S; UNCLASSIFIED DRUG; GALACTOSIDE 2-ALPHA-L-FUCOSYLTRANSFERASE;

ACTINOBACTERIA; ADULT; AMINO ACID METABOLISM; ARTICLE; BACTEROIDETES; COHORT ANALYSIS; DNA EXTRACTION; FECES ANALYSIS; FECES MICROFLORA; FEMALE; FIRMICUTES; GENE SEQUENCE; GENETIC ASSOCIATION; GENETIC VARIABILITY; GENOTYPE; HUMAN; INFLAMMATORY BOWEL DISEASE; INTESTINE FLORA; MAJOR CLINICAL STUDY; MALE; MICROBIAL COMMUNITY; MICROBIAL DIVERSITY; MICROBIAL IDENTIFICATION; NORMAL HUMAN; OPERATIONAL TAXONOMIC UNIT; PHENOTYPE; POLYMERASE CHAIN REACTION; PYROSEQUENCING; SINGLE NUCLEOTIDE POLYMORPHISM; TAXONOMIC IDENTIFICATION; ADOLESCENT; BACTERIUM; CLASSIFICATION; FECES; GENETICS; ISOLATION AND PURIFICATION; METABOLISM; MICROBIOLOGY; YOUNG ADULT;

ADOLESCENT; ADULT; BACTERIA; COHORT STUDIES; FECES; FEMALE; FUCOSYLTRANSFERASES; GASTROINTESTINAL MICROBIOME; GENOTYPE; HEALTHY VOLUNTEERS; HUMANS; MALE; PHENOTYPE; POLYMORPHISM, SINGLE NUCLEOTIDE; YOUNG ADULT;

EID: 85046025107     PISSN: 19490976     EISSN: 19490984     Source Type: Journal    
DOI: 10.1080/19490976.2018.1445956     Document Type: Article

References (56)

1. Sanz Y, Olivares M, Moya-Perez A, Agostoni C. Understanding the role of gut microbiome in metabolic disease risk. Pediatric research. 2015;77:236–44. doi:10.1038/pr.2014.170. PMID:25314581
2. Consortium THMP. Structure, Function and Diversity af the Healthy Human Microbiome. Nature. 2012;486:207–14. doi:10.1038/nature11234. PMID:22699609
3. Gorvitovskaia A, Holmes SP, Huse SM. Interpreting Prevotella and Bacteroides as biomarkers of diet and lifestyle. Microbiome. 2016;4:15. doi:10.1186/s40168-016-0160-7. PMID:27068581
4. Schloissnig S, Arumugam M, Sunagawa S, Mitreva M, Tap J, Zhu A, Waller A, Mende DR, Kultima JR, Martin J. Genomic variation landscape of the human gut microbiome. Nature. 2013;493:45–50. doi:10.1038/nature11711. PMID:23222524
5. 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. Proceedings of the National Academy of Sciences of the United States of America. 2010;107:14691–6. doi:10.1073/pnas.1005963107. PMID:20679230
6. Goodrich JK, Waters JL, Poole AC, Sutter JL, Koren O, Blekhman R, et al. Human genetics shape the gut microbiome. Cell. 2014;159:789–99. doi:10.1016/j.cell.2014.09.053. PMID:25417156
7. Turpin W, Espin-Garcia O, Xu W, Silverberg MS, Kevans D, Smith MI, Guttman DS, Griffiths A, Panaccione R, Otley A. Association of host genome with intestinal microbial composition in a large healthy cohort. Nature genetics. 2016;48:1413–7. doi:10.1038/ng.3693. PMID:27694960
8. Tong M, McHardy I, Ruegger P, Goudarzi M, Kashyap PC, Haritunians T, Li X, Graeber TG, Schwager E, Huttenhower C. Reprograming of Gut Microbiome Energy Metabolism by the Fut2 Crohn's Disease Risk Polymorphism. The ISME journal. 2014;8:2193–206. doi:10.1038/ismej.2014.64. PMID:24781901
9. Rausch P, Rehman A, Kunzel S, Hasler R, Ott SJ, Schreiber S, Rosenstiel P, Franke A, Baines JF. Colonic mucosa-associated microbiota is influenced by an interaction of Crohn disease and FUT2 (Secretor) genotype. Proceedings of the National Academy of Sciences of the United States of America. 2011;108:19030–5. doi:10.1073/pnas.1106408108. PMID:22068912
10. Wacklin P, Makivuokko H, Alakulppi N, Nikkila J, Tenkanen H, Rabina J, Partanen J, Aranko K, Mättö J. Secretor genotype (FUT2 gene) is strongly associated with the composition of Bifidobacteria in the human intestine. PloS one. 2011;6:e20113. doi:10.1371/journal.pone.0020113. PMID:21625510
11. Wacklin P, Tuimala J, Nikkila J, Sebastian T, Makivuokko H, Alakulppi N, Laine P, Rajilic-Stojanovic M, Paulin L, de Vos WM. Faecal microbiota composition in adults is associated with the FUT2 gene determining the secretor status. PloS one. 2014;9:e94863. doi:10.1371/journal.pone.0094863. PMID:24733310
12. Cleynen I, Boucher G, Jostins L, Schumm LP, Zeissig S, Ahmad T, Andersen V, Andrews JM, Annese V, Brand S. Inherited determinants of Crohn's disease and ulcerative colitis phenotypes: a genetic association study. Lancet (London, England). 2016;387:156–67. doi:10.1016/S0140-6736(15)00465-1. PMID:26490195
13. Jostins L, Ripke S, Weersma RK, Duerr RH, McGovern DP, Hui KY, Lee JC, Schumm LP, Sharma Y, Anderson CA. Host-microbe interactions have shaped the genetic architecture of inflammatory bowel disease. Nature. 2012;491:119–24. doi:10.1038/nature11582. PMID:23128233
14. McGovern DP, Jones MR, Taylor KD, Marciante K, Yan X, Dubinsky M, Ippoliti A, Vasiliauskas E, Berel D, Derkowski C. Fucosyltransferase 2 (FUT2) non-secretor status is associated with Crohn's disease. Human molecular genetics. 2010;19:3468–76. doi:10.1093/hmg/ddq248. PMID:20570966
15. Wu H, Sun L, Lin DP, Shao XX, Xia SL, Lv M. Association of Fucosyltransferase 2 Gene Polymorphisms with Inflammatory Bowel Disease in Patients from Southeast China. Gastroenterology research and practice. 2017;2017:4148651. doi:10.1155/2017/4148651. PMID:28167958
16. Bry L, Falk PG, Midtvedt T, Gordon JI. A model of host-microbial interactions in an open mammalian ecosystem. Science (New York, NY). 1996;273:1380–3. doi:10.1126/science.273.5280.1380
17. Meng D, Newburg DS, Young C, Baker A, Tonkonogy SL, Sartor RB, Walker WA, Nanthakumar NN. Bacterial symbionts induce a FUT2-dependent fucosylated niche on colonic epithelium via ERK and JNK signaling. American journal of physiology Gastrointestinal and liver physiology. 2007;293:G780–7. doi:10.1152/ajpgi.00010.2007. PMID:17673542
18. Pham, Tu, Anh, N, Clare S, Goulding D, Arasteh Julia M, Stares Mark D, Browne Hilary P, Page AJ, Kumasaka N, Kane L. Epithelial IL-22RA1-Mediated Fucosylation Promotes Intestinal Colonization Resistance to an Opportunistic Pathogen. Cell Host & Microbe. 2014;16:504–16. doi:10.1016/j.chom.2014.08.017
19. Pickard JM, Maurice CF, Kinnebrew MA, Abt MC, Schenten D, Golovkina TV, Bogatyrev SR, Ismagilov RF, Pamer EG, Turnbaugh PJ. Rapid fucosylation of intestinal epithelium sustains host-commensal symbiosis in sickness. Nature. 2014;514:638–41. doi:10.1038/nature13823. PMID:25274297
20. Folseraas T, Melum E, Rausch P, Juran BD, Ellinghaus E, Shiryaev A, Laerdahl JK, Ellinghaus D, Schramm C, Weismüller TJ. Extended analysis of a genome-wide association study in primary sclerosing cholangitis detects multiple novel risk loci. Journal of hepatology. 2012;57:366–75. doi:10.1016/j.jhep.2012.03.031. PMID:22521342
21. Goto Y, Obata T, Kunisawa J, Sato S, Ivanov II, Lamichhane A, Takeyama N, Kamioka M, Sakamoto M, Matsuki T. Innate Lymphoid Cells Regulate Intestinal Epithelial Cell Glycosylation. Science (New York, NY). 2014;345:1254009. doi:10.1126/science.1254009
22. Rausch P, Kunzel S, Suwandi A, Grassl GA, Rosenstiel P, Baines JF. Multigenerational Influences of the Fut2 Gene on the Dynamics of the Gut Microbiota in Mice. Frontiers in microbiology. 2017;8:991. doi:10.3389/fmicb.2017.00991. PMID:28642740
23. Kashyap PC, Marcobal A, Ursell LK, Smits SA, Sonnenburg ED, Costello EK, Higginbottom SK, Domino SE, Holmes SP, Relman DA. Genetically dictated change in host mucus carbohydrate landscape exerts a diet-dependent effect on the gut microbiota. Proceedings of the National Academy of Sciences of the United States of America. 2013;110:17059–64. doi:10.1073/pnas.1306070110. PMID:24062455
24. Huse SM, Ye Y, Zhou Y, Fodor AA. A core human microbiome as viewed through 16S rRNA sequence clusters. PloS one. 2012;7:e34242. doi:10.1371/journal.pone.0034242. PMID:22719824
25. Bokulich NA, Subramanian S, Faith JJ, Gevers D, Gordon JI, Knight R, Mills DA, Caporaso JG. Quality-filtering vastly improves diversity estimates from Illumina amplicon sequencing. Nature methods. 2013;10:57–9. doi:10.1038/nmeth.2276. PMID:23202435
26. Davenport ER, Goodrich JK, Bell JT, Spector TD, Ley RE, Clark AG. ABO antigen and secretor statuses are not associated with gut microbiota composition in 1,500 twins. BMC genomics. 2016;17:941. doi:10.1186/s12864-016-3290-1. PMID:27871240
27. Wang J, Thingholm LB, Skieceviciene J, Rausch P, Kummen M, Hov JR, Degenhardt F, Heinsen FA, Rühlemann MC, Szymczak S. Genome-wide association analysis identifies variation in vitamin D receptor and other host factors influencing the gut microbiota. Nature genetics. 2016;48:1396–406. doi:10.1038/ng.3695. PMID:27723756
28. Bonder MJ, Kurilshikov A, Tigchelaar EF, Mujagic Z, Imhann F, Vila AV, et al. The effect of host genetics on the gut microbiome. Nature genetics. 2016;48:1407–12. doi:10.1038/ng.3663. PMID:27694959
29. Langendijk PS, Schut F, Jansen GJ, Raangs GC, Kamphuis GR, Wilkinson MH, Welling GW. Quantitative fluorescence in situ hybridization of Bifidobacterium spp. with genus-specific 16S rRNA-targeted probes and its application in fecal samples. Applied and environmental microbiology. 1995;61:3069–75
30. Caporaso JG, Lauber CL, Walters WA, Berg-Lyons D, Huntley J, Fierer N, Owens SM, Betley J, Fraser L, Bauer M. Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms. The ISME journal. 2012;6:1621–4. doi:10.1038/ismej.2012.8. PMID:22402401
31. Group JCHMPDGW. Evaluation of 16S rDNA-based community profiling for human microbiome research. PloS one. 2012;7:e39315. doi:10.1371/journal.pone.0039315. PMID:22720093
32. Rodriguez-Diaz J, Garcia-Mantrana I, Vila-Vicent S, Gozalbo-Rovira R, Buesa J, Monedero V, Collado MC. Relevance of secretor status genotype and microbiota composition in susceptibility to rotavirus and norovirus infections in humans. Scientific reports. 2017;7:45559. doi:10.1038/srep45559. PMID:28358023
33. Smith MI, Turpin W, Tyler AD, Silverberg MS, Croitoru K. Microbiome analysis–from technical advances to biological relevance. F1000prime reports. 2014;6:51. doi:10.12703/P6-51. PMID:25184041
34. Langille MG, Zaneveld J, Caporaso JG, McDonald D, Knights D, Reyes JA, Clemente JC, Burkepile DE, Vega Thurber RL, Knight R. Predictive functional profiling of microbial communities using 16S rRNA marker gene sequences. Nature biotechnology. 2013;31:814–21. doi:10.1038/nbt.2676. PMID:23975157
35. Eckburg PB, Bik EM, Bernstein CN, Purdom E, Dethlefsen L, Sargent M, et al. Diversity of the human intestinal microbial flora. Science (New York, NY). 2005;308:1635–8. doi:10.1126/science.1110591
36. Holmen Larsson JM, Thomsson KA, Rodriguez-Pineiro AM, Karlsson H, Hansson GC. Studies of mucus in mouse stomach, small intestine, and colon. III. Gastrointestinal Muc5ac and Muc2 mucin O-glycan patterns reveal a regiospecific distribution. American journal of physiology Gastrointestinal and liver physiology. 2013;305:G357–63. doi:10.1152/ajpgi.00048.2013. PMID:23832516
37. Robbe C, Capon C, Coddeville B, Michalski JC. Structural diversity and specific distribution of O-glycans in normal human mucins along the intestinal tract. The Biochemical journal. 2004;384:307–16. doi:10.1042/BJ20040605. PMID:15361072
38. Hopkins MJ, Sharp R, Macfarlane GT. Variation in human intestinal microbiota with age. Digestive and liver disease: official journal of the Italian Society of Gastroenterology and the Italian Association for the Study of the Liver. 2002;34(Suppl 2):12–8. doi:10.1016/S1590-8658(02)80157-8. PMID:12408433
39. Kennedy NA, Walker AW, Berry SH, Duncan SH, Farquarson FM, Louis P, Thomson JM, Satsangi J, Flint HJ, Parkhill J. The impact of different DNA extraction kits and laboratories upon the assessment of human gut microbiota composition by 16S rRNA gene sequencing. PloS one. 2014;9:e88982. doi:10.1371/journal.pone.0088982. PMID:24586470
40. Lozupone CA, Stombaugh J, Gonzalez A, Ackermann G, Wendel D, Vazquez-Baeza Y, et al. Meta-analyses of studies of the human microbiota. Genome research. 2013;23:1704–14. doi:10.1101/gr.151803.112. PMID:23861384
41. Kevans D, Turpin W, Madsen K, Meddings J, Shestopaloff K, Xu W, Moreno-Hagelsieb G, Griffiths A, Silverberg MS, Paterson A. Determinants of intestinal permeability in healthy first-degree relatives of individuals with Crohn's disease. Inflammatory bowel diseases. 2015;21:879–87. doi:10.1097/MIB.0000000000000323. PMID:25734694
42. Ferrer-Admetlla A, Sikora M, Laayouni H, Esteve A, Roubinet F, Blancher A, Calafell F, Bertranpetit J, Casals F. A natural history of FUT2 polymorphism in humans. Molecular biology and evolution. 2009;26:1993–2003. doi:10.1093/molbev/msp108. PMID:19487333
43. The International Hap. Map Project. Nature. 2003;426:789–96. PMID:14685227
44. Masella AP, Bartram AK, Truszkowski JM, Brown DG, Neufeld JD. PANDAseq: paired-end assembler for illumina sequences. BMC bioinformatics. 2012;13:31. doi:10.1186/1471-2105-13-31. PMID:22333067
45. Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Peña AG, Goodrich JK, Gordon JI. QIIME allows analysis of high-throughput community sequencing data. Nature methods. 2010;7:335–6. doi:10.1038/nmeth.f.303. PMID:20383131
46. Edgar RC. Search and clustering orders of magnitude faster than BLAST. Bioinformatics (Oxford, England). 2010;26:2460–1. doi:10.1093/bioinformatics/btq461. PMID:20709691
47. 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. Applied and environmental microbiology. 2006;72:5069–72. doi:10.1128/AEM.03006-05. PMID:16820507
48. Whittaker RH. Evolution and Measurement of Species Diversity. Taxon. 1972;21:213–51. doi:10.2307/1218190
49. Gauderman WJ. Sample size requirements for matched case-control studies of gene-environment interaction. Statistics in medicine. 2002;21:35–50. doi:10.1002/sim.973. PMID:11782049
50. Tregouet DA, Ducimetiere P, Tiret L. Testing association between candidate-gene markers and phenotype in related individuals, by use of estimating equations. American journal of human genetics. 1997;61:189–99. doi:10.1086/513895. PMID:9246000
51. Lozupone C, Lladser M, Knights D, Stombaugh J, Knight R. UniFrac: an effective distance metric for microbial community comparison. The ISME journal. 2011;5:169–72. doi:10.1038/ismej.2010.133. PMID:20827291
52. Fierer N, Lauber CL, Zhou N, McDonald D, Costello EK, Knight R. Forensic identification using skin bacterial communities. Proceedings of the National Academy of Sciences of the United States of America. 2010;107:6477–81. doi:10.1073/pnas.1000162107. PMID:20231444
53. Paradis E, Claude J, Strimmer K. APE: Analyses of Phylogenetics and Evolution in R language. Bioinformatics (Oxford, England). 2004;20:289–90. doi:10.1093/bioinformatics/btg412. PMID:14734327
54. Kanehisa M, Goto S, Sato Y, Furumichi M, Tanabe M. KEGG for integration and interpretation of large-scale molecular data sets. Nucleic acids research. 2012;40:D109–14. doi:10.1093/nar/gkr988. PMID:22080510
55. Tatusov RL, Koonin EV, Lipman DJ. A genomic perspective on protein families. Science (New York, NY). 1997;278:631–7. doi:10.1126/science.278.5338.631
56. Gower JC. Generalized procrustes analysis. Psychometrika. 1975;40:33–51. doi:10.1007/BF02291478