Abstract
Many microbes are important symbiotes of human. They form specific microbiota communities, participate in various kinds of biological processes of their host and thus deeply affect human health status. Metagenomic sequencing has been widely used in human microbiota study due to its capacity of studying all genetic materials in an environment as a whole without any extra need of isolation or cultivation of microorganisms. Many efforts have been made by researchers in this area trying to dig out interesting knowledge from various metagenome data. In this review, we go through some prominent studies in the metagenomic area. We summarize them into three categories, constructing taxonomy and gene reference, characterization of microbiome distribution patterns, and detection of microbiome alternations associated with specific human phenotypes or diseases. Some available data resources are also provided. This review can serve as an entrance to this exciting and rapidly developing field for researchers interested in human microbiomes.
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Savage, D. C. (1977) Microbial ecology of the gastrointestinal tract. Annu. Rev. Microbiol., 31, 107–133
Lundberg, J. O., Weitzberg, E., Cole, J. A. and Benjamin, N. (2004) Nitrate, bacteria and human health. Nat. Rev. Microbiol., 2, 593–602
Relman, D. A. (2011) Microbial genomics and infectious diseases. N. Engl. J. Med., 365, 347–357
Loman, N. J., Constantinidou, C., Christner, M., Rohde, H., Chan, J. Z., Quick, J., Weir, J. C., Quince, C., Smith, G. P., Betley, J. R., et al. (2013) A culture-independent sequence-based metagenomics approach to the investigation of an outbreak of Shiga-toxigenic Escherichia coli O104:H4. JAMA, 309, 1502–1510
Kamada, N., Chen, G. Y., Inohara, N. and Núñez, G. (2013) Control of pathogens and pathobionts by the gut microbiota. Nat. Immunol., 14, 685–690.
Gallo, R. L. and Hooper, L. V. (2012) Epithelial antimicrobial defence of the skin and intestine. Nat. Rev. Immunol., 12, 503–516
Schloss, P. D. and Handelsman, J. (2005) Metagenomics for studying unculturable microorganisms: cutting the Gordian knot. Genome Biol., 6, 229
van Opstal, E. J. and Bordenstein, S. R. (2015) MICROBIOME. Rethinking heritability of the microbiome. Science, 349, 1172–1173
Handelsman, J., Rondon, M. R., Brady, S. F., Clardy, J. and Goodman, R. M. (1998) Molecular biological access to the chemistry of unknown soil microbes: a new frontier for natural products. Chem. Biol., 5, R245–R249
Sunagawa, S., Coelho, L. P., Chaffron, S., Kultima, J. R., Labadie, K., Salazar, G., Djahanschiri, B., Zeller, G., Mende, D. R., Alberti, A., et al. (2015) Ocean plankton. Structure and function of the global ocean microbiome. Science, 348, 1261359
Debroas, D., Humbert, J. F., Enault, F., Bronner, G., Faubladier, M. and Cornillot, E. (2009) Metagenomic approach studying the taxonomic and functional diversity of the bacterial community in a mesotrophic lake (Lac du Bourget—France). Environ. Microbiol., 11, 2412–2424
Rondon, M. R., August, P. R., Bettermann, A. D., Brady, S. F., Grossman, T. H., Liles, M. R., Loiacono, K. A., Lynch, B. A., MacNeil, I. A., Minor, C., et al. (2000) Cloning the soil metagenome: a strategy for accessing the genetic and functional diversity of uncultured microorganisms. Appl. Environ. Microbiol., 66, 2541–2547
Cesaroni, G., Forastiere, F., Stafoggia, M., Andersen, Z. J., Badaloni, C., Beelen, R., Caracciolo, B., de Faire, U., Erbel, R., Eriksen, K. T., et al. (2014) Long term exposure to ambient air pollution and incidence of acute coronary events: prospective cohort study and meta-analysis in 11 European cohorts from the ESCAPE Project. BMJ, 348, f7412
Walker, A. (2010) A glut from the gut: metagenomics takes a giant step foward. Nat. Rev. Microbiol., 8, 315
Lepage, P., Leclerc, M. C., Joossens, M., Mondot, S., Blottière, H. M., Raes, J., Ehrlich, D. and Doré, J. (2013) A metagenomic insight into our gut’s microbiome. Gut, 62, 146–158.
Quast, C., Pruesse, E., Yilmaz, P., Gerken, J., Schweer, T., Yarza, P., Peplies, J. and Glöckner, F. O. (2013) The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res., 41, D590–D596
DeSantis, T. Z., Hugenholtz, P., Larsen, N., Rojas, M., Brodie, E. L., Keller, K., Huber, T., Dalevi, D., Hu, P. and Andersen, G. L. (2006) Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Appl. Environ. Microbiol., 72, 5069–5072
Cole, J. R., Wang, Q., Fish, J. A., Chai, B., McGarrell, D. M., Sun, Y., Brown, C. T., Porras-Alfaro, A., Kuske, C. R. and Tiedje, J. M. (2014) Ribosomal Database Project: data and tools for high throughput rRNA analysis. Nucleic Acids Res., 42, D633–D642
NCBI Resource Coordinators. (2016) Database resources of the National Center for Biotechnology Information. Nucleic Acids Res., 44, D7–D19
Markowitz, V. M., Chen, I. M., Palaniappan, K., Chu, K., Szeto, E., Pillay, M., Ratner, A., Huang, J., Woyke, T., Huntemann, M., et al. (2014) IMG 4 version of the integrated microbial genomes comparative analysis system. Nucleic Acids Res., 42, D560–D567
Chen, T., Yu, W. H., Izard, J., Baranova, O. V., Lakshmanan, A. and Dewhirst, F. E. (2010) The Human Oral Microbiome Database: a web accessible resource for investigating oral microbe taxonomic and genomic information. Database (Oxford), 2010, baq013
Nielsen, H. B., Almeida, M., Juncker, A. S., Rasmussen, S., Li, J., Sunagawa, S., Plichta, D. R., Gautier, L., Pedersen, A. G., Le Chatelier, E., et al. (2014) Identification and assembly of genomes and genetic elements in complex metagenomic samples without using reference genomes. Nat. Biotechnol., 32, 822–828
Kanehisa, M., Sato, Y., Kawashima, M., Furumichi, M. and Tanabe, M. (2016) KEGG as a reference resource for gene and protein annotation. Nucleic Acids Res., 44, D457–D462
UniProt Consortium. (2015) UniProt: a hub for protein information. Nucleic Acids Res., 43, D204–D212
Huttenhower, C., Gevers, D., Knight, R., Abubucker, S., Badger, J. H., Chinwalla, A. T., Creasy, H. H., Earl, A. M., FitzGerald, M. G., Fulton, R. S., et al. (2012) Structure, function and diversity of the healthy human microbiome. Nature, 486, 207–214
Li, J., Jia, H., Cai, X., Zhong, H., Feng, Q., Sunagawa, S., Arumugam, M., Kultima, J. R., Prifti, E., Nielsen, T., et al. (2014) An integrated catalog of reference genes in the human gut microbiome. Nat. Biotechnol., 32, 834–841
Qin, N., Yang, F., Li, A., Prifti, E., Chen, Y., Shao, L., Guo, J., Le Chatelier, E., Yao, J., Wu, L., et al. (2014) Alterations of the human gut microbiome in liver cirrhosis. Nature, 513, 59–64
Oh, J., Byrd, A. L., Deming, C., Conlan, S., Kong, H. H., Segre, J. A., Segre, J. A., and the NISC Comparative Sequencing Program. (2014) Biogeography and individuality shape function in the human skin metagenome. Nature, 514, 59–64
Feng, Q., Liang, S., Jia, H., Stadlmayr, A., Tang, L., Lan, Z., Zhang, D., Xia, H., Xu, X., Jie, Z.,et al. (2015) Gut microbiome development along the colorectal adenoma-carcinoma sequence. Nat. Commun., 6, 6528
Meyer, F., Paarmann, D., D’Souza, M., Olson, R., Glass, E. M., Kubal, M., Paczian, T., Rodriguez, A., Stevens, R., Wilke, A., et al. (2008) The metagenomics RAST server—a public resource for the automatic phylogenetic and functional analysis of metagenomes. BMC Bioinformatics, 9, 386
Hunter, S., Corbett, M., Denise, H., Fraser, M., Gonzalez-Beltran, A., Hunter, C., Jones, P., Leinonen, R., McAnulla, C., Maguire, E., et al. (2014) EBI metagenomics—a new resource for the analysis and archiving of metagenomic data. Nucleic Acids Res., 42, D600–D606
Woese, C. R. (1987) Bacterial evolution. Microbiol. Rev., 51, 221–271
Stoddard, S. F., Smith, B. J., Hein, R., Roller, B. R. and Schmidt, T. M. (2015) rrnDB: improved tools for interpreting rRNA gene abundance in bacteria and archaea and a new foundation for future development. Nucleic Acids Res., 43, D593–D598
Li, H. and Durbin, R. (2009) Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics, 25, 1754–1760
Langmead, B. and Salzberg, S. L. (2012) Fast gapped-read alignment with Bowtie 2. Nat. Methods, 9, 357–359
Li, R., Yu, C., Li, Y., Lam, T. W., Yiu, S. M., Kristiansen, K. and Wang, J. (2009) SOAP2: an improved ultrafast tool for short read alignment. Bioinformatics, 25, 1966–1967
Methé, B. A., Nelson, K. E., Pop, M., Creasy, H. H., Giglio, M. G., Huttenhower, C., Gevers, D., Petrosino, J. F., Abubucker, S., Badger, J. H., et al. (2012) A framework for human microbiome research. Nature, 486, 215–221
Qin, J., Li, R., Raes, J., Arumugam, M., Burgdorf, K. S., Manichanh, C., Nielsen, T., Pons, N., Levenez, F., Yamada, T., et al. (2010) A human gut microbial gene catalogue established by metagenomic sequencing. Nature, 464, 59–65
Wood, D. E. and Salzberg, S. L. (2014) Kraken: ultrafast metagenomic sequence classification using exact alignments. Genome Biol., 15, R46
Jia, B., Xuan, L., Cai, K., Hu, Z., Ma, L. andWei, C. (2013) NeSSM: a next-generation sequencing simulator for metagenomics. PLoS One, 8, e75448
Qin, J., Li, Y., Cai, Z., Li, S., Zhu, J., Zhang, F., Liang, S., Zhang, W., Guan, Y., Shen, D., et al. (2012) A metagenome-wide association study of gut microbiota in type 2 diabetes. Nature, 490, 55–60
Baker, B. J., Sheik, C. S., Taylor, C. A., Jain, S., Bhasi, A., Cavalcoli, J. D. and Dick, G. J. (2013) Community transcriptomic assembly reveals microbes that contribute to deep-sea carbon and nitrogen cycling. ISME J., 7, 1962–1973
Inskeep, W. P., Jay, Z. J., Herrgard, M. J., Kozubal, M. A., Rusch, D. B., Tringe, S. G., Macur, R. E., Jennings, R., Boyd, E. S., Spear, J. R., et al. (2013) Phylogenetic and functional analysis of metagenome sequence from high-temperature archaeal habitats demonstrate linkages between metabolic potential and geochemistry. Front. Microbiol., 4, 95
Segata, N., Waldron, L., Ballarini, A., Narasimhan, V., Jousson, O. and Huttenhower, C. (2012) Metagenomic microbial community profiling using unique clade-specific marker genes. Nat. Methods, 9, 811–814
Jagtap, P., McGowan, T., Bandhakavi, S., Tu, Z. J., Seymour, S., Griffin, T. J. and Rudney, J. D. (2012) Deep metaproteomic analysis of human salivary supernatant. Proteomics, 12, 992–1001
Liu, B., Faller, L. L., Klitgord, N., Mazumdar, V., Ghodsi, M., Sommer, D. D., Gibbons, T. R., Treangen, T. J., Chang, Y. C., Li, S., et al. (2012) Deep sequencing of the oral microbiome reveals signatures of periodontal disease. PLoS One, 7, e37919
Warinner, C., Rodrigues, J. F., Vyas, R., Trachsel, C., Shved, N., Grossmann, J., Radini, A., Hancock, Y., Tito, R. Y., Fiddyment, S., et al. (2014) Pathogens and host immunity in the ancient human oral cavity. Nat. Genet., 46, 336–344
Luo, R., Liu, B., Xie, Y., Li, Z., Huang,W., Yuan, J., He, G., Chen, Y., Pan, Q., Liu, Y., et al. (2012) SOAPdenovo2: an empirically improved memory-efficient short-read de novo assembler. Gigascience, 1, 18
Namiki, T., Hachiya, T., Tanaka, H. and Sakakibara, Y. (2012) MetaVelvet: an extension of Velvet assembler to de novo metagenome assembly from short sequence reads. Nucleic Acids Res., 40, e155
Peng, Y., Leung, H. C., Yiu, S. M. and Chin, F. Y. (2011) Meta-IDBA: a de novo assembler for metagenomic data. Bioinformatics, 27, i94–i101
Zhu, W., Lomsadze, A. and Borodovsky, M. (2010) Ab initio gene identification in metagenomic sequences. Nucleic Acids Res., 38, e132
Delcher, A. L., Harmon, D., Kasif, S., White, O. and Salzberg, S. L. (1999) Improved microbial gene identification with GLIMMER. Nucleic Acids Res., 27, 4636–4641
Fu, L., Niu, B., Zhu, Z., Wu, S. and Li, W. (2012) CD-HIT: accelerated for clustering the next-generation sequencing data. Bioinformatics, 28, 3150–3152
Edgar, R. C. (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics, 26, 2460–2461
Le Chatelier, E., Nielsen, T., Qin, J., Prifti, E., Hildebrand, F., Falony, G., Almeida, M., Arumugam, M., Batto, J. M., Kennedy, S., et al. (2013) Richness of human gut microbiome correlates with metabolic markers. Nature, 500, 541–546
Tatusov, R. L., Koonin, E. V. and Lipman, D. J. (1997) A genomic perspective on protein families. Science, 278, 631–637
Overbeek, R., Begley, T., Butler, R. M., Choudhuri, J. V., Chuang, H. Y., Cohoon, M., de Crécy-Lagard, V., Diaz, N., Disz, T., Edwards, R., et al. (2005) The subsystems approach to genome annotation and its use in the project to annotate 1000 genomes. Nucleic Acids Res., 33, 5691–5702
Finn, R. D., Coggill, P., Eberhardt, R. Y., Eddy, S. R., Mistry, J., Mitchell, A. L., Potter, S. C., Punta, M., Qureshi, M., Sangrador-Vegas, A., et al. (2016) The Pfam protein families database: towards a more sustainable future. Nucleic Acids Res., 44, D279–D285
Selengut, J. D., Haft, D. H., Davidsen, T., Ganapathy, A., Gwinn-Giglio, M., Nelson, W. C., Richter, A. R. and White, O. (2007) TIGRFAMs and Genome Properties: tools for the assignment of molecular function and biological process in prokaryotic genomes. Nucleic Acids Res., 35, D260–D264
Huson, D. H., Auch, A. F., Qi, J. and Schuster, S. C. (2007) MEGAN analysis of metagenomic data. Genome Res., 17, 377–386
Zhou, X., Brown, C. J., Abdo, Z., Davis, C. C., Hansmann, M. A., Joyce, P., Foster, J. A. and Forney, L. J. (2007) Differences in the composition of vaginal microbial communities found in healthy Caucasian and black women. ISME J., 1, 121–133
Brotman, R. M., Bradford, L. L., Conrad, M., Gajer, P., Ault, K., Peralta, L., Forney, L. J., Carlton, J. M., Abdo, Z. and Ravel, J. (2012) Association between Trichomonas vaginalis and vaginal bacterial community composition among reproductive-age women. Sex. Transm. Dis., 39, 807–812
Brotman, R. M., Shardell, M. D., Gajer, P., Fadrosh, D., Chang, K., Silver, M. I., Viscidi, R. P., Burke, A. E., Ravel, J. and Gravitt, P. E. (2014) Association between the vaginal microbiota, menopause status, and signs of vulvovaginal atrophy. Menopause, 21, 450–458
Ravel, J., Gajer, P., Fu, L., Mauck, C. K., Koenig, S. S., Sakamoto, J., Motsinger-Reif, A. A., Doncel, G. F. and Zeichner, S. L. (2012) Twice-daily application of HIV microbicides alter the vaginal microbiota. MBio, 3, e00370–12
Mehta, S. D., Donovan, B., Weber, K. M., Cohen, M., Ravel, J., Gajer, P., Gilbert, D., Burgad, D. and Spear, G. T. (2015) The vaginal microbiota over an 8- to 10-year period in a cohort of HIV-infected and HIV-uninfected women. PLoS One, 10, e0116894
Romero, R., Hassan, S. S., Gajer, P., Tarca, A. L., Fadrosh, D. W., Nikita, L., Galuppi, M., Lamont, R. F., Chaemsaithong, P., Miranda, J., et al. (2014) The composition and stability of the vaginal microbiota of normal pregnant women is different from that of nonpregnant women. Microbiome, 2, 4
DiGiulio, D. B., Callahan, B. J., McMurdie, P. J., Costello, E. K., Lyell, D. J., Robaczewska, A., Sun, C. L., Goltsman, D. S., Wong, R. J., Shaw, G., et al. (2015) Temporal and spatial variation of the human microbiota during pregnancy. Proc. Natl. Acad. Sci. USA, 112, 11060–11065
Huang, Y. E., Wang, Y., He, Y., Ji, Y., Wang, L. P., Sheng, H. F., Zhang, M., Huang, Q. T., Zhang, D. J., Wu, J. J., et al. (2015) Homogeneity of the vaginal microbiome at the cervix, posterior fornix, and vaginal canal in pregnant Chinese women. Microb. Ecol., 69, 407–414
Arumugam, M., Raes, J., Pelletier, E., Le Paslier, D., Yamada, T., Mende, D. R., Fernandes, G. R., Tap, J., Bruls, T., Batto, J. M., et al. (2011) Enterotypes of the human gut microbiome. Nature, 473, 174–180
Wu, G. D., Chen, J., Hoffmann, C., Bittinger, K., Chen, Y. Y., Keilbaugh, S. A., Bewtra, M., Knights, D.,Walters,W. A., Knight, R., et al. (2011) Linking long-term dietary patterns with gut microbial enterotypes. Science, 334, 105–108
Moeller, A. H., Degnan, P. H., Pusey, A. E., Wilson, M. L., Hahn, B. H. and Ochman, H. (2012) Chimpanzees and humans harbour compositionally similar gut enterotypes. Nat. Commun., 3, 1179
Jeffery, I. B., Claesson, M. J., O’Toole, P. W. and Shanahan, F. (2012) Categorization of the gut microbiota: enterotypes or gradients? Nat. Rev. Microbiol., 10, 591–592
Knights, D., Ward, T. L., McKinlay, C. E., Miller, H., Gonzalez, A., McDonald, D. and Knight, R. (2014) Rethinking “enterotypes”. Cell Host Microbe, 16, 433–437
Ding, T. and Schloss, P. D. (2014) Dynamics and associations of microbial community types across the human body. Nature, 509, 357–360
Franzosa, E. A., Huang, K., Meadow, J. F., Gevers, D., Lemon, K. P., Bohannan, B. J. and Huttenhower, C. (2015) Identifying personal microbiomes using metagenomic codes. Proc. Natl. Acad. Sci. USA, 112, e2930–E2938
Sharon, I., Morowitz, M. J., Thomas, B. C., Costello, E. K., Relman, D. A. and Banfield, J. F. (2013) Time series community genomics analysis reveals rapid shifts in bacterial species, strains, and phage during infant gut colonization. Genome Res., 23, 111–120
Faith, J. J., Guruge, J. L., Charbonneau, M., Subramanian, S., Seedorf, H., Goodman, A. L., Clemente, J. C., Knight, R., Heath, A. C., Leibel, R. L., et al. (2013) The long-term stability of the human gut microbiota. Science, 341, 1237439
Lozupone, C. A., Stombaugh, J. I., Gordon, J. I., Jansson, J. K. and Knight, R. (2012) Diversity, stability and resilience of the human gut microbiota. Nature, 489, 220–230
David, L. A., Materna, A. C., Friedman, J., Campos-Baptista, M. I., Blackburn, M. C., Perrotta, A., Erdman, S. E. and Alm, E. J. (2014) Host lifestyle affects human microbiota on daily timescales. Genome Biol., 15, R89
Smith, M. I., Yatsunenko, T., Manary, M. J., Trehan, I., Mkakosya, R., Cheng, J., Kau, A. L., Rich, S. S., Concannon, P., Mychaleckyj, J. C., et al. (2013) Gut microbiomes of Malawian twin pairs discordant for kwashiorkor. Science, 339, 548–554
Dewulf, E. M., Cani, P. D., Claus, S. P., Fuentes, S., Puylaert, P. G., Neyrinck, A. M., Bindels, L. B., de Vos, W. M., Gibson, G. R., Thissen, J. P., et al. (2013) Insight into the prebiotic concept: lessons from an exploratory, double blind intervention study with inulin-type fructans in obese women. Gut, 62, 1112–1121
Cotillard, A., Kennedy, S. P., Kong, L. C., Prifti, E., Pons, N., Le Chatelier, E., Almeida, M., Quinquis, B., Levenez, F., Galleron, N., et al. (2013) Dietary intervention impact on gut microbial gene richness. Nature, 500, 585–588
Adler, C.J., Dobney, K., Weyrich, L.S., Kaidonis, J., Walker, A.W., Haak, W., Bradshaw, C.J., Townsend, G., Soltysiak, A., Alt, K.W. et al. (2013) Sequencing ancient calcified dental plaque shows changes in oral microbiota with dietary shifts of the Neolithic and Industrial revolutions. Nat Genet, 45, 450–455, 455e451
David, L. A., Maurice, C. F., Carmody, R. N., Gootenberg, D. B., Button, J. E., Wolfe, B. E., Ling, A. V., Devlin, A. S., Varma, Y., Fischbach, M. A., et al. (2014) Diet rapidly and reproducibly alters the human gut microbiome. Nature, 505, 559–563
Karlsson, F. H., Tremaroli, V., Nookaew, I., Bergström, G., Behre, C. J., Fagerberg, B., Nielsen, J. and Bäckhed, F. (2013) Gut metagenome in European women with normal, impaired and diabetic glucose control. Nature, 498, 99–103
Rajilic-Stojanovic, M., Biagi, E., Heilig, H. G., Kajander, K., Kekkonen, R. A., Tims, S. and de Vos, W. M. (2011) Global and deep molecular analysis of microbiota signatures in fecal samples from patients with irritable bowel syndrome. Gastroenterology, 141, 1792–1801
Saulnier, D. M., Riehle, K., Mistretta, T. A., Diaz, M. A., Mandal, D., Raza, S., Weidler, E. M., Qin, X., Coarfa, C., Milosavljevic, A., et al. (2011) Gastrointestinal microbiome signatures of pediatric patients with irritable bowel syndrome. Gastroenterology, 141, 1782–1791
Gevers, D., Kugathasan, S., Denson, L. A., Vá zquez-Baeza, Y., van Treuren, W., Ren, B., Schwager, E., Knights, D., Song, S. J., Yassour, M., et al. (2014) The treatment-naive microbiome in new-onset Crohn’s disease. Cell Host Microbe, 15, 382–392
Zhu, L., Baker, S. S., Gill, C., Liu, W., Alkhouri, R., Baker, R. D. and Gill, S. R. (2013) Characterization of gut microbiomes in nonalcoholic steatohepatitis (NASH) patients: a connection between endogenous alcohol and NASH. Hepatology, 57, 601–609
Karlsson, F. H., Fåk, F., Nookaew, I., Tremaroli, V., Fagerberg, B., Petranovic, D., Bäckhed, F. and Nielsen, J. (2012) Symptomatic atherosclerosis is associated with an altered gut metagenome. Nat. Commun., 3, 1245
Kostic, A. D., Gevers, D., Pedamallu, C. S., Michaud, M., Duke, F., Earl, A. M., Ojesina, A. I., Jung, J., Bass, A. J., Tabernero, J., et al. (2012) Genomic analysis identifies association of Fusobacterium with colorectal carcinoma. Genome Res., 22, 292–298
Yu, J., Feng, Q., Wong, S. H., Zhang, D., Liang, Q. Y., Qin, Y., Tang, L., Zhao, H., Stenvang, J., Li, Y., et al. (2015) Metagenomic analysis of faecal microbiome as a tool towards targeted non-invasive biomarkers for colorectal cancer. Gut, gutjnl-2015-309800
Tyakht, A. V., Kostryukova, E. S., Popenko, A. S., Belenikin, M. S., Pavlenko, A. V., Larin, A. K., Karpova, I. Y., Selezneva, O. V., Semashko, T. A., Ospanova, E. A., et al. (2013) Human gut microbiota community structures in urban and rural populations in Russia. Nat. Commun., 4, 2469
Koren, O., Goodrich, J. K., Cullender, T. C., Spor, A., Laitinen, K., Bäckhed, H. K., Gonzalez, A., Werner, J. J., Angenent, L. T., Knight, R., et al. (2012) Host remodeling of the gut microbiome and metabolic changes during pregnancy. Cell, 150, 470–480
Belda-Ferre, P., Alcaraz, L. D., Cabrera-Rubio, R., Romero, H., Simó n-Soro, A., Pignatelli, M. and Mira, A. (2012) The oral metagenome in health and disease. ISME J., 6, 46–56
Wang, J., Qi, J., Zhao, H., He, S., Zhang, Y., Wei, S. and Zhao, F. (2013) Metagenomic sequencing reveals microbiota and its functional potential associated with periodontal disease. Sci. Rep., 3, 1843
Duran-Pinedo, A. E., Chen, T., Teles, R., Starr, J. R., Wang, X., Krishnan, K. and Frias-Lopez, J. (2014) Community-wide transcriptome of the oral microbiome in subjects with and without periodontitis. ISME J., 8, 1659–1672
Yang, L., Lu, X., Nossa, C. W., Francois, F., Peek, R. M. and Pei, Z. (2009) Inflammation and intestinal metaplasia of the distal esophagus are associated with alterations in the microbiome. Gastroenterology, 137, 588–59
Tunney, M. M., Einarsson, G. G., Wei, L., Drain, M., Klem, E. R., Cardwell, C., Ennis, M., Boucher, R. C., Wolfgang, M. C. and Elborn, J. S. (2013) Lung microbiota and bacterial abundance in patients with bronchiectasis when clinically stable and during exacerbation. Am. J. Respir. Crit. Care Med., 187, 1118–1126
Marri, P.R., Stern, D.A., Wright, A.L., Billheimer, D. and Martinez, F. D. (2013) Asthma-associated differences in microbial composition of induced sputum. J. Allergy. Clin. Immunol., 131, 346–352. e3
Morris, A., Beck, J. M., Schloss, P. D., Campbell, T. B., Crothers, K., Curtis, J. L., Flores, S. C., Fontenot, A. P., Ghedin, E., Huang, L., et al. (2013) Comparison of the respiratory microbiome in healthy nonsmokers and smokers. Am. J. Respir. Crit. Care Med., 187, 1067–1075
Yatsunenko, T., Rey, F. E., Manary, M. J., Trehan, I., Dominguez- Bello, M. G., Contreras, M., Magris, M., Hidalgo, G., Baldassano, R. N., Anokhin, A. P., et al. (2012) Human gut microbiome viewed across age and geography. Nature, 486, 222–227.
Claesson, M. J., Jeffery, I. B., Conde, S., Power, S. E., O’Connor, E. M., Cusack, S., Harris, H. M., Coakley, M., Lakshminarayanan, B., O’Sullivan, O., et al. (2012) Gut microbiota composition correlates with diet and health in the elderly. Nature, 488, 178–184
Stahringer, S. S., Clemente, J. C., Corley, R. P., Hewitt, J., Knights, D., Walters, W. A., Knight, R. and Krauter, K. S. (2012) Nurture trumps nature in a longitudinal survey of salivary bacterial communities in twins from early adolescence to early adulthood. Genome Res., 22, 2146–2152
Lozupone, C. A., Stombaugh, J., Gonzalez, A., Ackermann, G., Wendel, D., Vá zquez-Baeza, Y., Jansson, J. K., Gordon, J. I. and Knight, R. (2013) Meta-analyses of studies of the human microbiota. Genome Res., 23, 1704–1714
Lax, S., Smith, D. P., Hampton-Marcell, J., Owens, S. M., Handley, K. M., Scott, N. M., Gibbons, S. M., Larsen, P., Shogan, B. D., Weiss, S., et al. (2014) Longitudinal analysis of microbial interaction between humans and the indoor environment. Science, 345, 1048–1052
Kuleshov, V., Jiang, C., Zhou, W., Jahanbani, F., Batzoglou, S. and Snyder, M. (2016) Synthetic long-read sequencing reveals intraspecies diversity in the human microbiome. Nat. Biotechnol., 34, 64–69
Forslund, K., Hildebrand, F., Nielsen, T., Falony, G., Le Chatelier, E., Sunagawa, S., Prifti, E., Vieira-Silva, S., Gudmundsdottir, V., Krogh Pedersen, H., et al. (2015) Disentangling type 2 diabetes and metformin treatment signatures in the human gut microbiota. Nature, 528, 262–266
Liu, S., da Cunha, A. P., Rezende, R. M., Cialic, R., Wei, Z., Bry, L., Comstock, L. E., Gandhi, R. andWeiner, H. L. (2016) The host shapes the gut microbiota via fecal microRNA. Cell Host Microbe., 19, 32–43
Cui, H. and Zhang, X. (2013) Alignment-free supervised classification of metagenomes by recursive SVM. BMC Genomics, 14, 641
Jiang, B., Song, K., Ren, J., Deng, M., Sun, F. and Zhang, X. (2012) Comparison of metagenomic samples using sequence signatures. BMC Genomics, 13, 730
Wang, Y., Liu, L., Chen, L., Chen, T. and Sun, F. (2014) Comparison of metatranscriptomic samples based on k-tuple frequencies. PLoS One, 9, e84348
Reyes, A., Haynes, M., Hanson, N., Angly, F. E., Heath, A. C., Rohwer, F. and Gordon, J. I. (2010) Viruses in the faecal microbiota of monozygotic twins and their mothers. Nature, 466, 334–338
Kuss, S. K., Best, G. T., Etheredge, C. A., Pruijssers, A. J., Frierson, J. M., Hooper, L. V., Dermody, T. S. and Pfeiffer, J. K. (2011) Intestinal microbiota promote enteric virus replication and systemic pathogenesis. Science, 334, 249–252
Minot, S., Sinha, R., Chen, J., Li, H., Keilbaugh, S. A., Wu, G. D., Lewis, J. D. and Bushman, F. D. (2011) The human gut virome: interindividual variation and dynamic response to diet. Genome Res., 21, 1616–1625
Minot, S., Bryson, A., Chehoud, C., Wu, G. D., Lewis, J. D. and Bushman, F. D. (2013) Rapid evolution of the human gut virome. Proc. Natl. Acad. Sci. USA, 110, 12450–12455
Edlund, A., Santiago-Rodriguez, T.M., Boehm, T.K. and Pride, D.T. (2015) Bacteriophage and their potential roles in the human oral cavity. 2015, 27423
Wang, J., Gao, Y. and Zhao, F. (2015) Phage-bacteria interaction network in human oral microbiome. Environ. Microbiol, 10.1111/1462-2920.12923
Bisanz, J. E. and Reid, G. (2011) Unraveling how probiotic yogurt works. Sci. Transl. Med., 3, 106ps41
Ghishan, F. K. and Kiela, P. R. (2011) From probiotics to therapeutics: another step forward? J. Clin. Invest., 121, 2149–2152
Borody, T. J. and Khoruts, A. (2012) Fecal microbiota transplantation and emerging applications. Nat. Rev. Gastroenterol. Hepatol., 9, 88–96
Lemon, K. P., Armitage, G. C., Relman, D. A. and Fischbach, M. A. (2012) Microbiota-targeted therapies: an ecological perspective. Sci. Transl. Med., 4, 137rv5
Sonnenburg, E. D., Smits, S. A., Tikhonov, M., Higginbottom, S. K., Wingreen, N. S. and Sonnenburg, J. L. (2016) Diet-induced extinctions in the gut microbiota compound over generations. Nature, 529, 212–215
Chevalier, C., Stojanovic, O., Colin, D. J., Suarez-Zamorano, N., Tarallo, V., Veyrat-Durebex, C., Rigo, D., Fabbiano, S., Stevanovic, A., Hagemann, S., et al. (2015) Gut microbiota orchestrates energy homeostasis during cold. Cell, 163, 1360–1374
Zhang, X., Liu, S., Cui, H. and Chen, T.Reading the underlying information from massive metagenome sequencing data. To be published.
Bajaj, J. S., Betrapally, N. S. and Gillevet, P. M. (2015) Decompensated cirrhosis and microbiome interpretation. Nature, 525, e1–E2
Dubilier, N., McFall-Ngai, M. and Zhao, L. (2015) Microbiology: Create a global microbiome effort. Nature, 526, 631–634
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This article is dedicated to the Special Collection of Recent Advances in Next-Generation Bioinformatics (Ed. Xuegong Zhang).
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Cui, H., Li, Y. & Zhang, X. An overview of major metagenomic studies on human microbiomes in health and disease. Quant Biol 4, 192–206 (2016). https://doi.org/10.1007/s40484-016-0078-x
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DOI: https://doi.org/10.1007/s40484-016-0078-x