Host genetic variation and its microbiome interactions within the Human Microbiome Project

Genome Medicine

Volumn 10, Issue 1, 2018, Pages

  Kolde, Raivo ^a   Franzosa, Eric A ^b,c   Rahnavard, Gholamali ^b,c   Hall, Andrew Brantley ^c   Vlamakis, Hera ^c   Stevens, Christine ^c   Daly, Mark J ^a,c   Xavier, Ramnik J ^a,c,d   Huttenhower, Curtis ^b,c  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

^b HARVARD SCHOOL OF PUBLIC HEALTH   (United States)

^c BROAD INSTITUTE OF MIT AND HARVARD   (United States)

^d Massachusetts Institute of Technology   (United States)

Author keywords

Association studies; Human genome sequence; Human Microbiome Project; Microbiome and human genetics; Microbiome metagenome sequence

Indexed keywords

GENOMIC DNA;

ADULT; ARTICLE; BIFIDOBACTERIUM LONGUM; DNA SEQUENCE; FECES MICROFLORA; FEMALE; FUT2 GENE; GENE; GENETIC VARIATION; HOST PATHOGEN INTERACTION; HUMAN; HUMAN GENOME; HUMAN MICROBIOME PROJECT; INDEL MUTATION; INTESTINE FLORA; LACTASE DEFICIENCY; LCT GENE; MALE; MEDICAL RESEARCH; METAGENOME; MOUTH FLORA; NONHUMAN; PRIORITY JOURNAL; SINGLE NUCLEOTIDE POLYMORPHISM; VAGINA FLORA; WHOLE GENOME SEQUENCING; DONOR; GENETICS; GENOTYPE; MICROFLORA; PRINCIPAL COMPONENT ANALYSIS;

GENETIC VARIATION; GENOTYPE; HUMANS; METAGENOME; MICROBIOTA; PRINCIPAL COMPONENT ANALYSIS; SEQUENCE ANALYSIS, DNA; TISSUE DONORS;

EID: 85041177384     PISSN: None     EISSN: 1756994X     Source Type: Journal    
DOI: 10.1186/s13073-018-0515-8     Document Type: Article

References (60)

1. Human Microbiome Project C. Structure, function and diversity of the healthy human microbiome. Nature. 2012;486:207-14.
2. Pham TA, Clare S, Goulding D, Arasteh JM, Stares MD, Browne HP, Keane JA, Page AJ, Kumasaka N, Kane L, et al. Epithelial IL-22RA1-mediated fucosylation promotes intestinal colonization resistance to an opportunistic pathogen. Cell Host Microbe. 2014;16:504-16.
3. Aujoulat F, Bouvet P, Jumas-Bilak E, Jean-Pierre H, Marchandin H. Veillonella seminalis sp. nov., a novel anaerobic Gram-stain-negative coccus from human clinical samples, and emended description of the genus Veillonella. Int J Syst Evol Microbiol. 2014;64:3526-31.
4. Rodrigues NF, Kastle J, Coutinho TJ, Amorim AT, Campos GB, Santos VM, Marques LM, Timenetsky J, de Farias ST. Qualitative analysis of the vaginal microbiota of healthy cattle and cattle with genital-tract disease. Genet Mol Res. 2015;14:6518-28.
5. Kevans D, Turpin W, Madsen K, Meddings J, Shestopaloff K, Xu W, Moreno-Hagelsieb G, Griffiths A, Silverberg MS, Paterson A, et al. Determinants of intestinal permeability in healthy first-degree relatives of individuals with Crohn's disease. Inflamm Bowel Dis. 2015;21:879-87.
6. Brito IL, Yilmaz S, Huang K, Xu L, Jupiter SD, Jenkins AP, Naisilisili W, Tamminen M, Smillie CS, Wortman JR, et al. Mobile genes in the human microbiome are structured from global to individual scales. Nature. 2016;535:435-9.
7. Mao B, Li D, Zhao J, Liu X, Gu Z, Chen YQ, Zhang H, Chen W. In vitro fermentation of fructooligosaccharides with human gut bacteria. Food Funct. 2015;6:947-54.
8. Williams BB, Van Benschoten AH, Cimermancic P, Donia MS, Zimmermann M, Taketani M, Ishihara A, Kashyap PC, Fraser JS, Fischbach MA. Discovery and characterization of gut microbiota decarboxylases that can produce the neurotransmitter tryptamine. Cell Host Microbe. 2014;16:495-503.
9. Oh J, Byrd AL, Deming C, Conlan S, Program NCS, Kong HH, Segre JA. Biogeography and individuality shape function in the human skin metagenome. Nature. 2014;514:59-64.
10. Warinner C, Rodrigues JF, Vyas R, Trachsel C, Shved N, Grossmann J, Radini A, Hancock Y, Tito RY, Fiddyment S, et al. Pathogens and host immunity in the ancient human oral cavity. Nat Genet. 2014;46:336-44.
11. Forslund K, Sunagawa S, Kultima JR, Mende DR, Arumugam M, Typas A, Bork P. Country-specific antibiotic use practices impact the human gut resistome. Genome Res. 2013;23:1163-9.
12. Oh J, Byrd AL, Park M, Program NCS, Kong HH, Segre JA. Temporal stability of the human skin microbiome. Cell. 2016;165:854-66.
13. David LA, Materna AC, Friedman J, Campos-Baptista MI, Blackburn MC, Perrotta A, Erdman SE, Alm EJ. Host lifestyle affects human microbiota on daily timescales. Genome Biol. 2014;15:R89.
14. Ding T, Schloss PD. Dynamics and associations of microbial community types across the human body. Nature. 2014;509:357-60.
15. Benson AK, Kelly SA, Legge R, Ma F, Low SJ, Kim J, Zhang M, Oh PL, Nehrenberg D, Hua K, et al. Individuality in gut microbiota composition is a complex polygenic trait shaped by multiple environmental and host genetic factors. Proc Natl Acad Sci U S A. 2010;107:18933-8.
16. Leamy LJ, Kelly SA, Nietfeldt J, Legge RM, Ma F, Hua K, Sinha R, Peterson DA, Walter J, Benson AK, Pomp D. Host genetics and diet, but not immunoglobulin A expression, converge to shape compositional features of the gut microbiome in an advanced intercross population of mice. Genome Biol. 2014;15:552.
17. Org E, Parks BW, Joo JW, Emert B, Schwartzman W, Kang EY, Mehrabian M, Pan C, Knight R, Gunsalus R, et al. Genetic and environmental control of host-gut microbiota interactions. Genome Res. 2015;25:1558-69.
18. Falony G, Joossens M, Vieira-Silva S, Wang J, Darzi Y, Faust K, Kurilshikov A, Bonder MJ, Valles-Colomer M, Vandeputte D, et al. Population-level analysis of gut microbiome variation. Science. 2016;352:560-4.
19. Zhernakova A, Kurilshikov A, Bonder MJ, Tigchelaar EF, Schirmer M, Vatanen T, Mujagic Z, Vila AV, Falony G, Vieira-Silva S, et al. Population-based metagenomics analysis reveals markers for gut microbiome composition and diversity. Science. 2016;352:565-9.
20. Davenport ER, Cusanovich DA, Michelini K, Barreiro LB, Ober C, Gilad Y. Genome-wide association studies of the human gut microbiota. PLoS One. 2015;10:e0140301.
21. Hansen EE, Lozupone CA, Rey FE, Wu M, Guruge JL, Narra A, Goodfellow J, Zaneveld JR, McDonald DT, Goodrich JA, et al. Pan-genome of the dominant human gut-associated archaeon, Methanobrevibacter smithii, studied in twins. Proc Natl Acad Sci U S A. 2011;108 Suppl 1:4599-606.
22. Goodrich JK, Davenport ER, Beaumont M, Jackson MA, Knight R, Ober C, Spector TD, Bell JT, Clark AG, Ley RE. Genetic determinants of the gut microbiome in UK twins. Cell Host Microbe. 2016;19:731-43.
23. Turpin W, Espin-Garcia O, Xu W, Silverberg MS, Kevans D, Smith MI, Guttman DS, Griffiths A, Panaccione R, Otley A, et al. Association of host genome with intestinal microbial composition in a large healthy cohort. Nat Genet. 2016;48(11):1413-7.
24. Knights D, Silverberg MS, Weersma RK, Gevers D, Dijkstra G, Huang H, Tyler AD, van Sommeren S, Imhann F, Stempak JM, et al. Complex host genetics influence the microbiome in inflammatory bowel disease. Genome Med. 2014;6:107.
25. Blekhman R, Goodrich JK, Huang K, Sun Q, Bukowski R, Bell JT, Spector TD, Keinan A, Ley RE, Gevers D, Clark AG. Host genetic variation impacts microbiome composition across human body sites. Genome Biol. 2015;16:191.
26. Bonder MJ, Kurilshikov A, Tigchelaar EF, Mujagic Z, Imhann F, Vila AV, Deelen P, Vatanen T, Schirmer M, Smeekens SP, et al. The effect of host genetics on the gut microbiome. Nat Genet. 2016;48(11):1407-12.
27. Wacklin P, Makivuokko H, Alakulppi N, Nikkila J, Tenkanen H, Rabina J, Partanen J, Aranko K, Matto J. Secretor genotype (FUT2 gene) is strongly associated with the composition of Bifidobacteria in the human intestine. PLoS One. 2011;6:e20113.
28. Zhang X, Zhang D, Jia H, Feng Q, Wang D, Liang D, Wu X, Li J, Tang L, Li Y, et al. The oral and gut microbiomes are perturbed in rheumatoid arthritis and partly normalized after treatment. Nat Med. 2015;21:895-905.
29. Gevers D, Kugathasan S, Denson LA, Vazquez-Baeza Y, Van Treuren W, Ren B, Schwager E, Knights D, Song SJ, Yassour M, et al. The treatment-naive microbiome in new-onset Crohn's disease. Cell Host Microbe. 2014;15:382-92.
30. Ma J, Coarfa C, Qin X, Bonnen PE, Milosavljevic A, Versalovic J, Aagaard K. mtDNA haplogroup and single nucleotide polymorphisms structure human microbiome communities. BMC Genomics. 2014;15:257.
31. Genomes Project C, Auton A, Brooks LD, Durbin RM, Garrison EP, Kang HM, Korbel JO, Marchini JL, McCarthy S, McVean GA, Abecasis GR. A global reference for human genetic variation. Nature. 2015;526:68-74.
32. Genome of the Netherlands Consortium. Whole-genome sequence variation, population structure and demographic history of the Dutch population. Nat Genet. 2014;46:818-25.
33. Li H, Durbin R. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics. 2009;25:1754-60.
34. Li H. Toward better understanding of artifacts in variant calling from high-coverage samples. Bioinformatics. 2014;30:2843-51.
35. McLaren W, Pritchard B, Rios D, Chen Y, Flicek P, Cunningham F. Deriving the consequences of genomic variants with the Ensembl API and SNP Effect Predictor. Bioinformatics. 2010;26:2069-70.
36. Chang CC, Chow CC, Tellier LC, Vattikuti S, Purcell SM, Lee JJ. Second-generation PLINK: rising to the challenge of larger and richer datasets. Gigascience. 2015;4:7.
37. Manichaikul A, Mychaleckyj JC, Rich SS, Daly K, Sale M, Chen WM. Robust relationship inference in genome-wide association studies. Bioinformatics. 2010;26:2867-73.
38. Gevers D, Pop M, Schloss PD, Huttenhower C. Bioinformatics for the Human Microbiome Project. PLoS Comput Biol. 2012;8:e1002779.
39. Lloyd-Price J, Mahurkar A, Rahnavard G, Crabtree J, Orvis J, Hall AB, Brady A, Creasy HH, McCracken C, Giglio MG, et al. Strains, functions and dynamics in the expanded Human Microbiome Project. Nature. 2017;550(7674):61-6.
40. Truong DT, Franzosa EA, Tickle TL, Scholz M, Weingart G, Pasolli E, Tett A, Huttenhower C, Segata N. MetaPhlAn2 for enhanced metagenomic taxonomic profiling. Nat Methods. 2015;12:902-3.
41. Huang K, Brady A, Mahurkar A, White O, Gevers D, Huttenhower C, Segata N. MetaRef: a pan-genomic database for comparative and community microbial genomics. Nucleic Acids Res. 2014;42:D617-624.
42. Suzek BE, Wang Y, Huang H, McGarvey PB, Wu CH, UniProt Consortium. UniRef clusters: a comprehensive and scalable alternative for improving sequence similarity searches. Bioinformatics. 2015;31:926-32.
43. Caspi R, Billington R, Ferrer L, Foerster H, Fulcher CA, Keseler IM, Kothari A, Krummenacker M, Latendresse M, Mueller LA, et al. The MetaCyc database of metabolic pathways and enzymes and the BioCyc collection of pathway/genome databases. Nucleic Acids Res. 2016;44:D471-480.
44. Abubucker S, Segata N, Goll J, Schubert AM, Izard J, Cantarel BL, Rodriguez-Mueller B, Zucker J, Thiagarajan M, Henrissat B, et al. Metabolic reconstruction for metagenomic data and its application to the human microbiome. PLoS Comput Biol. 2012;8:e1002358.
45. Kolde R, Laur S, Adler P, Vilo J. Robust rank aggregation for gene list integration and meta-analysis. Bioinformatics. 2012;28:573-80.
46. Shabalin AA. Matrix eQTL: ultra fast eQTL analysis via large matrix operations. Bioinformatics. 2012;28:1353-8.
47. Human Microbiome Project C. A framework for human microbiome research. Nature. 2012;486:215-21.
48. Kelly RJ, Rouquier S, Giorgi D, Lennon GG, Lowe JB. Sequence and expression of a candidate for the human Secretor blood group alpha(1,2)fucosyltransferase gene (FUT2). Homozygosity for an enzyme-inactivating nonsense mutation commonly correlates with the non-secretor phenotype. J Biol Chem. 1995;270:4640-9.
49. Enattah NS, Sahi T, Savilahti E, Terwilliger JD, Peltonen L, Jarvela I. Identification of a variant associated with adult-type hypolactasia. Nat Genet. 2002;30:233-7.
50. Welter D, MacArthur J, Morales J, Burdett T, Hall P, Junkins H, Klemm A, Flicek P, Manolio T, Hindorff L, Parkinson H. The NHGRI GWAS Catalog, a curated resource of SNP-trait associations. Nucleic Acids Res. 2014;42:D1001-1006.
51. Consortium GT. Human genomics. The Genotype-Tissue Expression (GTEx) pilot analysis: multitissue gene regulation in humans. Science. 2015;348:648-60.
52. Goodrich JK, Waters JL, Poole AC, Sutter JL, Koren O, Blekhman R, Beaumont M, Van Treuren W, Knight R, Bell JT, et al. Human genetics shape the gut microbiome. Cell. 2014;159:789-99.
53. Baulieu EE, Thomas G, Legrain S, Lahlou N, Roger M, Debuire B, Faucounau V, Girard L, Hervy MP, Latour F, et al. Dehydroepiandrosterone (DHEA), DHEA sulfate, and aging: contribution of the DHEAge Study to a sociobiomedical issue. Proc Natl Acad Sci U S A. 2000;97:4279-84.
54. Jostins L, Ripke S, Weersma RK, Duerr RH, McGovern DP, Hui KY, Lee JC, Schumm LP, Sharma Y, Anderson CA, et al. Host-microbe interactions have shaped the genetic architecture of inflammatory bowel disease. Nature. 2012;491:119-24.
55. Kirino Y, Bertsias G, Ishigatsubo Y, Mizuki N, Tugal-Tutkun I, Seyahi E, Ozyazgan Y, Sacli FS, Erer B, Inoko H, et al. Genome-wide association analysis identifies new susceptibility loci for Behcet's disease and epistasis between HLA-B*51 and ERAP1. Nat Genet. 2013;45:202-7.
56. Genetic Analysis of Psoriasis Consortium, the Wellcome Trust Case Control Consortium, Strange A, Capon F, Spencer CC, Knight J, Weale ME, Allen MH, Barton A, Band G, et al. A genome-wide association study identifies new psoriasis susceptibility loci and an interaction between HLA-C and ERAP1. Nat Genet. 2010;42:985-90.
57. Li YR, Li J, Zhao SD, Bradfield JP, Mentch FD, Maggadottir SM, Hou C, Abrams DJ, Chang D, Gao F, et al. Meta-analysis of shared genetic architecture across ten pediatric autoimmune diseases. Nat Med. 2015;21:1018-27.
58. Nagaoka K, Izumikawa K, Yamamoto Y, Yanagihara K, Ohkusu K, Kohno S. Multiple lung abscesses caused by Actinomyces graevenitzii mimicking acute pulmonary coccidioidomycosis. J Clin Microbiol. 2012;50:3125-8.
59. Costello ME, Ciccia F, Willner D, Warrington N, Robinson PC, Gardiner B, Marshall M, Kenna TJ, Triolo G, Brown MA. Intestinal dysbiosis in ankylosing spondylitis. Arthritis Rheumatol. 2015;67:686-91.
60. Evans DM, Spencer CC, Pointon JJ, Su Z, Harvey D, Kochan G, Oppermann U, Dilthey A, Pirinen M, Stone MA, et al. Interaction between ERAP1 and HLA-B27 in ankylosing spondylitis implicates peptide handling in the mechanism for HLA-B27 in disease susceptibility. Nat Genet. 2011;43:761-7.