Metagenome-wide association studies: Fine-mining the microbiome

Nature Reviews Microbiology

Volumn 14, Issue 8, 2016, Pages 508-522

  Wang, Jun ^a,b   Jia, Huijue ^b  

^a Shahe Industrial Zone ^*  (China)

^b BGI SHENZHEN   (China)

Author keywords

[No Author keywords available]

Indexed keywords

BIOSYNTHESIS; COLORECTAL CANCER; DISEASE ASSOCIATION; ENVIRONMENTAL FACTOR; GENETIC LINKAGE; GENETIC RISK; GENETIC VARIABILITY; GENOME-WIDE ASSOCIATION STUDY; HUMAN; INTESTINE FLORA; LIVER CIRRHOSIS; METAGENOMICS; MICROBIOME; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; OBESITY; OXIDATIVE STRESS; PHENOTYPE; PRIORITY JOURNAL; REVIEW; RHEUMATOID ARTHRITIS; ARTHRITIS, RHEUMATOID; BACTERIUM; COLORECTAL NEOPLASMS; DIABETES MELLITUS, TYPE 2; GASTROINTESTINAL TRACT; GENETICS; HIGH THROUGHPUT SEQUENCING; METAGENOME; MICROBIOLOGY; MICROFLORA; RECEIVER OPERATING CHARACTERISTIC;

RNA 16S;

ARTHRITIS, RHEUMATOID; BACTERIA; COLORECTAL NEOPLASMS; DIABETES MELLITUS, TYPE 2; GASTROINTESTINAL TRACT; GENOME-WIDE ASSOCIATION STUDY; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; HUMANS; LIVER CIRRHOSIS; METAGENOME; MICROBIOTA; OBESITY; RNA, RIBOSOMAL, 16S; ROC CURVE;

EID: 84978127724     PISSN: 17401526     EISSN: 17401534     Source Type: Journal    
DOI: 10.1038/nrmicro.2016.83     Document Type: Review

References (120)

1. Qin, J. et al. A human gut microbial gene catalogue established by metagenomic sequencing. Nature 464, 59-65 (2010).
2. Methé, B. A. et al. A framework for human microbiome research. Nature 486, 215-221 (2012).
3. Li, J. et al. An integrated catalog of reference genes in the human gut microbiome. Nat. Biotechnol. 32, 834-841 (2014).
4. Clemente, J. C., Ursell, L. K., Parfrey, L. W. & Knight, R. The impact of the gut microbiota on human health: an integrative view. Cell 148, 1258-1270 (2012).
5. Sommer, F. & Bäckhed, F. The gut microbiota - masters of host development and physiology. Nat. Rev. Microbiol. 11 , 227-238 (2013).
6. Marchesi, J. R. et al. The gut microbiota and host health: a new clinical frontier. Gut 65, 330-339 (2015).
7. Xu, Y. et al. Prevalence and control of diabetes in Chinese adults. JAMA 310, 948-959 (2013).
8. Larsen, N. et al. Gut microbiota in human adults with type 2 diabetes differs from non-diabetic adults. PLoS ONE 5, e9085 (2010).
9. Qin, J. et al. A metagenome-wide association study of gut microbiota in type 2 diabetes. Nature 490, 55-60 (2012).
10. Brubaker, P. L. & Anini, Y. Direct and indirect mechanisms regulating secretion of glucagon-like peptide-1 and glucagon-like peptide-2. Can. J. Physiol. Pharmacol. 81, 1005-1012 (2003).
11. Zhou, J. et al. Peptide YY and proglucagon mRNA expression patterns and regulation in the gut. Obesity (Silver Spring) 14, 683-689 (2006).
12. Sun, J. et al. Pancreatic β-cells limit autoimmune diabetes via an immunoregulatory antimicrobial peptide expressed under the influence of the gut microbiota. Immunity 43, 304-317 (2015).
13. Karlsson, F. H. et al. Gut metagenome in European women with normal, impaired and diabetic glucose control. Nature 498, 99-103 (2013).
14. Pyra, K. A., Saha, D. C. & Reimer, R. A. Prebiotic fiber increases hepatic acetyl CoA carboxylase phosphorylation and suppresses glucose-dependent insulinotropic polypeptide secretion more effectively when used with metformin in obese rats. J. Nutr. 142, 213-220 (2012).
15. Forslund, K. et al. Disentangling type 2 diabetes and metformin treatment signatures in the human gut microbiota. Nature 528, 262-266 (2015).
16. Shin, N.-R. et al. An increase in the Akkermansia spp. population induced by metformin treatment improves glucose homeostasis in diet-induced obese mice. Gut 63, 727-735 (2014).
17. Lee, H. & Ko, G. Effect of metformin on metabolic improvement and gut microbiota. Appl. Environ. Microbiol. 80, 5935-5943 (2014).
18. Le Chatelier, E. et al. Richness of human gut microbiome correlates with metabolic markers. Nature 500, 541-546 (2013).
19. Cotillard, A. et al. Dietary intervention impact on gut microbial gene richness. Nature 500, 585-588 (2013).
20. Ley, R. E., Turnbaugh, P. J., Klein, S. & Gordon, J. I. Microbial ecology: human gut microbes associated with obesity. Nature 444, 1022-1023 (2006).
21. Turnbaugh, P. J. et al. A core gut microbiome in obese and lean twins. Nature 457, 480-484 (2009).
22. Jemal, A. et al. Global cancer statistics. CA Cancer J. Clin. 61, 69-90 (2011).
23. Ferlay, J. et al. Cancer incidence and mortality worldwide: sources, methods and major patterns in GLOBOCAN 2012. Int. J. Cancer 136, E359-E386 (2015).
24. Brenner, H., Kloor, M. & Pox, C. P. Colorectal cancer. Lancet 383, 1490-1502 (2014).
25. Kostic, A. D. et al. Genomic analysis identifies association of Fusobacterium with colorectal carcinoma. Genome Res. 22, 292-298 (2012).
26. Castellarin, M. et al. Fusobacterium nucleatum infection is prevalent in human colorectal carcinoma. Genome Res. 22, 299-306 (2012).
27. Kostic, A. D. et al. Fusobacterium nucleatum potentiates intestinal tumorigenesis and modulates the tumor-immune microenvironment. Cell Host Microbe 14, 207-215 (2013).
28. Gur, C. et al. Binding of the Fap2 protein of Fusobacterium nucleatum to human inhibitory receptor TIGIT protects tumors from immune cell attack. Immunity 42, 344-355 (2015).
29. Cho, I. & Blaser, M. J. The human microbiome: at the interface of health and disease. Nat. Rev. Genet. 13, 260-270 (2012).
30. Weir, T. L. et al. Stool microbiome and metabolome differences between colorectal cancer patients and healthy adults. PLoS ONE 8, e70803 (2013).
31. Zeller, G. et al. Potential of fecal microbiota for early-stage detection of colorectal cancer. Mol. Syst. Biol. 10, 766 (2014).
32. Feng, Q. et al. Gut microbiome development along the colorectal adenoma-carcinoma sequence. Nat. Commun. 6, 6528 (2015).
33. Yu, J. et al. Metagenomic analysis of faecal microbiome as a tool towards targeted non-invasive biomarkers for colorectal cancer. Gut http://dx.doi. org/10.1136/gutjnl-2015-309800 (2015).
34. Marchesi, J. R. et al. Towards the human colorectal cancer microbiome. PLoS ONE 6, e20447 (2011).
35. Nakatsu, G. et al. Gut mucosal microbiome across stages of colorectal carcinogenesis. Nat. Commun. 6, 8727 (2015).
36. Tjalsma, H., Boleij, A., Marchesi, J. R. & Dutilh, B. E. A bacterial driver-passenger model for colorectal cancer: beyond the usual suspects. Nat. Rev. Microbiol. 10, 575-582 (2012).
37. Louis, P. , Hold, G. L. & Flint, H. J. The gut microbiota, bacterial metabolites and colorectal cancer. Nat. Rev. Microbiol. 12, 661-672 (2014).
38. Iida, N. et al. Commensal bacteria control cancer response to therapy by modulating the tumor microenvironment. Science 342, 967-970 (2013).
39. Viaud, S. et al. The intestinal microbiota modulates the anticancer immune effects of cyclophosphamide. Science 342, 971-976 (2013).
40. Schwabe, R. F. & Jobin, C. The microbiome and cancer. Nat. Rev. Cancer 13, 800-812 (2013).
41. Vetizou, M. et al. Anticancer immunotherapy by CTLA-4 blockade relies on the gut microbiota. Science 350, 1079-1084 (2015).
42. Sivan, A. et al. Commensal Bifidobacterium promotes antitumor immunity and facilitates anti-PD-L1 efficacy. Science 350, 1084-1089 (2015).
43. McInnes, I. B. & Schett, G. The pathogenesis of rheumatoid arthritis. N. Engl. J. Med. 365, 2205-2219 (2011).
44. Demoruelle, M. K., Deane, K. D. & Holers, V. M. When and where does inflammation begin in rheumatoid arthritis? Curr. Opin. Rheumatol. 26, 2264-2271 (2014).
45. Zhang, X. et al. The oral and gut microbiomes are perturbed in rheumatoid arthritis and partly normalized after treatment. Nat. Med. 21, 895-905 (2015).
46. Scher, J. U. et al. Expansion of intestinal Prevotella copri correlates with enhanced susceptibility to arthritis. eLife 2, e01202 (2013).
47. Scher, J. U. et al. Periodontal disease and the oral microbiota in new-onset rheumatoid arthritis. Arthritis Rheum. 64, 3083-3094 (2012).
48. Deane, K. D. & El-Gabalawy, H. Pathogenesis and prevention of rheumatic disease: focus on preclinical RA and SLE. Nat. Rev. Rheumatol. 10, 212-228 (2014).
49. Karlsson, F. H. et al. Symptomatic atherosclerosis is associated with an altered gut metagenome. Nat. Commun. 3, 1245 (2012).
50. Fu, J. et al. The gut microbiome contributes to a substantial proportion of the variation in blood lipids. Circ. Res. 11 7 , 817-824 (2015).
51. Qin, N. et al. Alterations of the human gut microbiome in liver cirrhosis. Nature 513, 859-864 (2014).
52. Ding, T. & Schloss, P. D. Dynamics and associations of microbial community types across the human body. Nature 509, 357-360 (2014).
53. Bäckhed, F. et al. Dynamics and stabilization of the human gut microbiome during the first year of life. Cell Host Microbe 17, 690-703 (2015).
54. Sonnenburg, J. L. et al. Glycan foraging in vivo by an intestine-adapted bacterial symbiont. Science 307, 1955-1959 (2005).
55. Koropatkin, N. M., Cameron, E. A. & Martens, E. C. How glycan metabolism shapes the human gut microbiota. Nat. Rev. Microbiol. 10, 323-335 (2012).
56. Kashnap, P. et al. Genetically dictated change in host mucus carbohydrate landscape exerts a diet-dependent effect on gut microbiota. Proc. Natl Acad. Sci. USA 110, 17059-17064 (2013).
57. Lee, S. M. et al. Bacterial colonization factors control specificity and stability of the gut microbiota. Nature 501, 426-429 (2013).
58. Motta, J.-P. et al. Hydrogen sulfide protects from colitis and restores intestinal microbiota biofilm and mucus production. Inflamm. Bowel Dis. 21, 1006-1017 (2015).
59. Benson, A. 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. USA 107, 18933-18938 (2010).
60. Benson, A. K. Host genetic architecture and the landscape of microbiome composition: humans weigh in. Genome Biol. 16, 203 (2015).
61. Goodrich, J. K. et al. Human genetics shape the gut microbiome. Cell 159, 789-799 (2014).
62. van Opstal, E. J. & Bordenstein, S. R. Rethinking heritability of the microbiome. Science 349, 1172-1173 (2015).
63. Rausch, P. et al. Colonic mucosa-associated microbiota is influenced by an interaction of Crohn disease and FUT2 (Secretor) genotype. Proc. Natl Acad. Sci. USA 108, 19030-19035 (2011).
64. Pickard, J. M. et al. Rapid fucosylation of intestinal epithelium sustains host-commensal symbiosis in sickness. Nature 514, 638-641 (2014).
65. Goto, Y. et al. Innate lymphoid cells regulate intestinal epithelial cell glycosylation. Science 345, 1254009 (2014).
66. Franzosa, E. A. et al. Sequencing and beyond: integrating molecular 'omics' for microbial community profiling. Nat. Rev. Microbiol. 13, 360-372 (2015).
67. Sridharan, G. V. et al. Prediction and quantification of bioactive microbiota metabolites in the mouse gut. Nat. Commun. 5, 5492 (2014).
68. Shoaie, S. et al. Quantifying diet-induced metabolic changes of the human gut microbiome. Cell. Metab. 22, 320-331 (2015).
69. Xu, J. et al. Structural modulation of gut microbiota during alleviation of type 2 diabetes with a Chinese herbal formula. ISME J. 9, 552-562 (2014).
70. Lukens, J. R. et al. Dietary modulation of the microbiome affects autoinflammatory disease. Nature 516, 246-249 (2014).
71. Hsiao, E. Y. et al. Microbiota modulate behavioral and physiological abnormalities associated with neurodevelopmental disorders. Cell 155, 1451-1463 (2013).
72. reg induction by a rationally selected mixture of Clostridia strains from the human microbiota. Nature 500, 232-236 (2013).
73. Ridaura, V. K. et al. Gut microbiota from twins discordant for obesity modulate metabolism in mice. Science 341, 1241214 (2013).
74. Xiao, L. et al. A catalog of the mouse gut metagenome. Nat. Biotechnol. 33, 1103-1108 (2015).
75. Bäckhed, F., Manchester, J. K., Semenkovich, C. F. & Gordon, J. I. Mechanisms underlying the resistance to diet-induced obesity in germ-free mice. Proc. Natl Acad. Sci. USA 104, 979-984 (2007).
76. Mukherji, A., Kobiita, A., Ye, T. & Chambon, P. Homeostasis in intestinal epithelium is orchestrated by the circadian clock and microbiota cues transduced by TLRs. Cell 153, 812-827 (2013).
77. Olszak, T. et al. Microbial exposure during early life has persistent effects on natural killer T cell function. Science 336, 489-493 (2012).
78. Braniste, V. et al. The gut microbiota influences blood-brain barrier permeability in mice. Sci. Transl Med. 6, 263ra158 (2014).
79. Erny, D. et al. Host microbiota constantly control maturation and function of microglia in the CNS. Nat. Neurosci. 18, 965-977 (2015).
80. Lacombe, A. et al. Lowbush wild blueberries have the potential to modify gut microbiota and xenobiotic metabolism in the rat colon. PLoS ONE 8, e67497 (2013).
81. Hildebrand, F. et al. A comparative analysis of the intestinal metagenomes present in guinea pigs (Cavia porcellus) and humans (Homo sapiens). BMC Genomics 13, 514 (2012).
82. Cabreiro, F. & Gems, D. Worms need microbes too: microbiota, health and aging in Caenorhabditis elegans. EMBO Mol. Med. 5, 1300-1310 (2013).
83. Turnbaugh, P. J. et al. An obesity-associated gut microbiome with increased capacity for energy harvest. Nature 444, 1027-1031 (2006).
84. Lukovac, S. et al. Differential modulation by Akkermansia muciniphila and Faecalibacterium prausnitzii of host peripheral lipid metabolism and histone acetylation in mouse gut organoids. mBio 5, e01438-14 (2014).
85. Kim, K., Lee, S. & Ryu, C.-M. Interspecific bacterial sensing through airborne signals modulates locomotion and drug resistance. Nat. Commun. 4, 1809 (2013).
86. Cuskin, F. et al. Human gut Bacteroidetes can utilize yeast mannan through a selfish mechanism. Nature 517, 165-169 (2015).
87. Stowell, S. R. et al. Microbial glycan microarrays define key features of host-microbial interactions. Nat. Chem. Biol. 10, 470-476 (2014).
88. Wang, X. et al. Cloning and variation of ground state intestinal stem cells. Nature 522, 173-178 (2015).
89. Joice, R., Yasuda, K., Shafquat, A., Morgan, X. C. & Huttenhower, C. Determining microbial products and identifying molecular targets in the human microbiome. Cell. Metab. 20, 731-741 (2014).
90. Dobkin, J. F., Saha, J. R., Butler, V. P. , Neu, H. C. & Lindenbaum, J. Inactivation of digoxin by Eubacterium lentum, an anaerobe of the human gut flora. Trans. Assoc. Am. Physicians 95, 22-29 (1982).
91. Haiser, H. J. et al. Predicting and manipulating cardiac drug inactivation by the human gut bacterium Eggerthella lenta. Science 341, 295-298 (2013).
92. Albertsen, M. et al. Genome sequences of rare, uncultured bacteria obtained by differential coverage binning of multiple metagenomes. Nat. Biotechnol. 31, 533-538 (2013).
93. Nielsen, H. B. et al. Identification and assembly of genomes and genetic elements in complex metagenomic samples without using reference genomes. Nat. Biotechnol. 32, 822-828 (2014).
94. Kuleshov, V. et al. Synthetic long-read sequencing reveals intraspecies diversity in the human microbiome. Nat. Biotechnol. 34, 64-69 (2015).
95. McLean, J. S. et al. Candidate phylum TM6 genome recovered from a hospital sink biofilm provides genomic insights into this uncultivated phylum. Proc. Natl Acad. Sci. USA 110 , E2390-E2399 (2013).
96. Rinke, C. et al. Insights into the phylogeny and coding potential of microbial dark matter. Nature 499, 431-437 (2013).
97. Reyes, A. et al. Viruses in the faecal microbiota of monozygotic twins and their mothers. Nature 466, 334-338 (2010).
98. Smillie, C. S. et al. Ecology drives a global network of gene exchange connecting the human microbiome. Nature 480, 241-244 (2011).
99. Minot, S. et al. The human gut virome: interindividual variation and dynamic response to diet. Genome Res. 21, 1616-1625 (2011).
100. Modi, S. R., Lee, H. H., Spina, C. S. & Collins, J. J. Antibiotic treatment expands the resistance reservoir and ecological network of the phage metagenome. Nature 499, 219-222 (2013).
101. Norman, J. M. et al. Disease-specific alterations in the enteric virome in inflammatory bowel disease. Cell 160, 447-460 (2015).
102. Schloissnig, S. et al. Genomic variation landscape of the human gut microbiome. Nature 493, 45-50 (2012).
103. Hu, Y. et al. Metagenome-wide analysis of antibiotic resistance genes in a large cohort of human gut microbiota. Nat. Commun. 4, 2151 (2013).
104. Greenblum, S., Carr, R. & Borenstein, E. Extensive strain-level copy-number variation across human gut microbiome species. Cell 160, 583-594 (2015).
105. Aagaard, K. et al. The placenta harbors a unique microbiome. Sci. Transl Med. 6, 237ra65 (2014).
106. Oh, J. et al. Biogeography and individuality shape function in the human skin metagenome. Nature 514, 59-64 (2014).
107. Kultima, J. R. et al. MOCAT: a metagenomics assembly and gene prediction toolkit. PLoS ONE 7, e47656 (2012).
108. Human Microbiome Project Consortium. Structure, function and diversity of the healthy human microbiome. Nature 486, 207-214 (2012).
109. Arumugam, M. et al. Enterotypes of the human gut microbiome. Nature 473, 174-180 (2011).
110. Sunagawa, S. et al. Metagenomic species profiling using universal phylogenetic marker genes. Nat. Methods 10, 1196-1199 (2013).
111. Mende, D. R., Sunagawa, S., Zeller, G. & Bork, P. Accurate and universal delineation of prokaryotic species. Nat. Methods 10, 881-884 (2013).
112. Dupont, C. L. et al. Genomic insights to SAR86, an abundant and uncultivated marine bacterial lineage. ISME J. 6, 1186-1199 (2012).
113. Freitas, T. A., Li, P.-E., Scholz, M. B. & Chain, P. S. Accurate read-based metagenome characterization using a hierarchical suite of unique signatures. Nucleic Acids Res. 43, e69 (2015).
114. Spanogiannopoulos, P., Bess, E. N., Carmody, R. N. & Turnbaugh, P. J. The microbial pharmacists within us: a metagenomic view of xenobiotic metabolism. Nat. Rev. Microbiol. 14, 273-287 (2016).
115. Gill, S. & Panda, S. A. Smartphone app reveals erratic diurnal eating patterns in humans that can be modulated for health benefits. Cell. Metab. 22, 789-798 (2015).
116. Kovatcheva-Datchary, P. et al. Dietary fiber-induced improvement in glucose metabolism is associated with increased abundance of Prevotella. Cell. Metab. 22, 971-982 (2015).
117. Zeevi, D. et al. Personalized nutrition by prediction of glycemic responses. Cell 163, 1079-1094 (2015).
118. Olle, B. Medicines from microbiota. Nat. Biotechnol. 31, 309-315 (2013).
119. Ling, L. L. et al. A new antibiotic kills pathogens without detectable resistance. Nature 517, 455-459 (2015).
120. Wang, Z. et al. Non-lethal inhibition of gut microbial trimethylamine production for the treatment of atherosclerosis. Cell 163, 1585-1595 (2015).