Meta'omic analytic techniques for studying the intestinal microbiome

Gastroenterology

Volumn 146, Issue 6, 2014, Pages

  Morgan, Xochitl C ^a,b   Huttenhower, Curtis ^a,b  

^a HARVARD SCHOOL OF PUBLIC HEALTH   (United States)

^b MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

Metagenomics; Metatranscriptomics; Microbiome; Tools

Indexed keywords

GENOMIC DNA; RNA 16S; TRANSCRIPTOME;

ACTINOBACTERIA; AKKERMANSIA; ARTICLE; BACTEROIDETES; BIOINFORMATICS; CANDIDA; CORYNEBACTERIUM; DYSBIOSIS; ENTEROBACTERIACEAE; ESCHERICHIA; EUBACTERIUM; FAECALIBACTERIUM; FIRMICUTES; FUSOBACTERIA; HUMAN; INFLAMMATORY BOWEL DISEASE; INTESTINE FLORA; LACHNOSPIRACEAE; LACTOBACILLUS; META ANALYSIS (TOPIC); METABOLOMICS; METAGENOME; METAGENOMICS; METAPROTEOMICS; METATRANSCRIPTOMICS; METHANOBREVIBACTER; MICROBIAL COMMUNITY; NONHUMAN; NUCLEOTIDE SEQUENCE; PASTEURELLACEAE; PRIORITY JOURNAL; PROTEOBACTERIA; PROTEOMICS; RNA GENE; STATISTICAL ANALYSIS; STREPTOCOCCUS; TRANSCRIPTOMICS;

METAGENOMICS; METATRANSCRIPTOMICS; MICROBIOME; TOOLS;

ANIMALS; BACTERIA; DNA, BACTERIAL; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, BACTERIAL; GENOTYPE; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; HOST-PATHOGEN INTERACTIONS; HUMANS; INFLAMMATORY BOWEL DISEASES; INTESTINES; METAGENOME; METAGENOMICS; MICROBIOTA; MODELS, STATISTICAL; PHENOTYPE; PHYLOGENY; RIBOTYPING; RNA, BACTERIAL; RNA, RIBOSOMAL, 16S; TRANSCRIPTOME;

EID: 84898808700     PISSN: 00165085     EISSN: 15280012     Source Type: Journal    
DOI: 10.1053/j.gastro.2014.01.049     Document Type: Article

References (114)

1. D.C. Savage Microbial ecology of the gastrointestinal tract Ann Rev Microbiol 31 1977 107 133
2. A. Sboner, X.J. Mu, and D. Greenbaum et al. The real cost of sequencing: higher than you think! Genome Biol 12 2011 125
3. J. Qin, R. Li, and J. Raes et al. A human gut microbial gene catalogue established by metagenomic sequencing Nature 464 2010 59 65
4. Human Microbiome Project Consortium Structure, function and diversity of the healthy human microbiome Nature 486 2012 207 214
5. C.R. Woese, G.E. Fox, and L. Zablen et al. Conservation of primary structure in 16S ribosomal RNA Nature 254 1975 83 86
6. M. Margulies, M. Egholm, and W.E. Altman et al. Genome sequencing in microfabricated high-density picolitre reactors Nature 437 2005 376 380
7. M.L. Sogin, H.G. Morrison, and J.A. Huber et al. Microbial diversity in the deep sea and the underexplored "rare biosphere" Proc Natl Acad Sci U S A 103 2006 12115 12120
8. D.R. Bentley, S. Balasubramanian, and H.P. Swerdlow et al. Accurate whole human genome sequencing using reversible terminator chemistry Nature 456 2008 53 59
9. V. Lazarevic, K. Whiteson, and S. Huse et al. Metagenomic study of the oral microbiota by Illumina high-throughput sequencing J Microbiol Methods 79 2009 266 271
10. M. Hamady, and R. Knight Microbial community profiling for human microbiome projects: tools, techniques, and challenges Genome Res 19 2009 1141 1152
11. Jumpstart Consortium Human Microbiome Project Data Generation Working Group Evaluation of 16S rDNA-based community profiling for human microbiome research PLoS One 7 2012 e39315
12. P.H. Degnan, and H. Ochman Illumina-based analysis of microbial community diversity ISME J 6 2012 183 194
13. J. Kuczynski, J. Stombaugh, and W.A. Walters et al. Using QIIME to analyze 16S rRNA gene sequences from microbial communities Curr Protoc Microbiol 2012 Chapter 1:Unit 1E 5
14. J.J. Kozich, S.L. Westcott, and N.T. Baxter et al. Development of a dual-index sequencing strategy and curation pipeline for analyzing amplicon sequence data on the MiSeq Illumina sequencing platform Appl Environ Microbiol 79 2013 5112 5120
15. J.G. Caporaso, J. Kuczynski, and J. Stombaugh et al. QIIME allows analysis of high-throughput community sequencing data Nat Methods 7 2010 335 336
16. P.D. Schloss, S.L. Westcott, and T. Ryabin et al. Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities Appl Environ Microbiol 75 2009 7537 7541
17. C. Quince, A. Lanzen, and R.J. Davenport et al. Removing noise from pyrosequenced amplicons BMC Bioinformatics 12 2011 38
18. B.P. Willing, J. Dicksved, and J. Halfvarson et al. A pyrosequencing study in twins shows that gastrointestinal microbial profiles vary with inflammatory bowel disease phenotypes Gastroenterology 139 2010 1844 1854.e1
19. M. Joossens, G. Huys, and M. Cnockaert et al. Dysbiosis of the faecal microbiota in patients with Crohn's disease and their unaffected relatives Gut 60 2011 631 637
20. N. Segata, J. Izard, and L. Waldron et al. Metagenomic biomarker discovery and explanation Genome Biol 12 2011 R60
21. C.K. Lee, C.W. Herbold, and S.W. Polson et al. Groundtruthing next-gen sequencing for microbial ecology-biases and errors in community structure estimates from PCR amplicon pyrosequencing PLoS One 7 2012 e44224
22. P.J. Turnbaugh, C. Quince, and J.J. Faith et al. Organismal, genetic, and transcriptional variation in the deeply sequenced gut microbiomes of identical twins Proc Natl Acad Sci U S A 107 2010 7503 7508
23. M.G. Langille, J. Zaneveld, and J.G. Caporaso et al. Predictive functional profiling of microbial communities using 16S rRNA marker gene sequences Nat Biotechnol 31 2013 814 821
24. R.H. Nilsson, E. Kristiansson, and M. Ryberg et al. Intraspecific ITS variability in the kingdom fungi as expressed in the international sequence databases and its implications for molecular species identification Evol Bioinform Online 4 2008 193 201
25. C. Hoffmann, S. Dollive, and S. Grunberg et al. Archaea and fungi of the human gut microbiome: correlations with diet and bacterial residents PLoS One 8 2013 e66019
26. T.L. Tickle, N. Segata, and L. Waldron et al. Two-stage microbial community experimental design ISME J 7 2013 2330 2339
27. J.L. Morgan, A.E. Darling, and J.A. Eisen Metagenomic sequencing of an in vitro-simulated microbial community PLoS One 5 2010 e10209
28. A. Reyes, N.P. Semenkovich, and K. Whiteson et al. Going viral: next-generation sequencing applied to phage populations in the human gut Nat Rev Microbiol 10 2012 607 617
29. A. Reyes, M. Haynes, and N. Hanson et al. Viruses in the faecal microbiota of monozygotic twins and their mothers Nature 466 2010 334 338
30. I.D. Iliev, V.A. Funari, and K.D. Taylor et al. Interactions between commensal fungi and the C-type lectin receptor Dectin-1 influence colitis Science 336 2012 1314 1317
31. S. Minot, R. Sinha, and J. Chen et al. The human gut virome: inter-individual variation and dynamic response to diet Genome Res 21 2011 1616 1625
32. S.R. Modi, H.H. Lee, and C.S. Spina et al. Antibiotic treatment expands the resistance reservoir and ecological network of the phage metagenome Nature 499 2013 219 222
33. Z. Zhang, C. Li, and X. Zhao et al. Anti-Saccharomyces cerevisiae antibodies associate with phenotypes and higher risk for surgery in Crohn's disease: a meta-analysis Dig Dis Sci 57 2012 2944 2954
34. T.B. Murdoch, W. Xu, and J.M. Stempak et al. Pattern recognition receptor and autophagy gene variants are associated with development of antimicrobial antibodies in Crohn's disease Inflamm Bowel Dis 18 2012 1743 1748
35. T. Vetrovsky, and P. Baldrian The variability of the 16S rRNA gene in bacterial genomes and its consequences for bacterial community analyses PLoS One 8 2013 e57923
36. H. Christensen, S. Nordentoft, and J.E. Olsen Phylogenetic relationships of Salmonella based on rRNA sequences Int J Syst Bacteriol 48 1998 605 610
37. N. Segata, and C. Huttenhower Toward an efficient method of identifying core genes for evolutionary and functional microbial phylogenies PLoS One 6 2011 e24704
38. A. Brady, and S.L. Salzberg Phymm and PhymmBL: metagenomic phylogenetic classification with interpolated Markov models Nat Methods 6 2009 673 676
39. S. Boisvert, F. Raymond, and E. Godzaridis et al. Ray Meta: scalable de novo metagenome assembly and profiling Genome Biol 13 2012 R122
40. N. Segata, D. Bornigen, and X.C. Morgan et al. PhyloPhlAn is a new method for improved phylogenetic and taxonomic placement of microbes Nat Commun 4 2013 2304
41. S. Schloissnig, M. Arumugam, and S. Sunagawa et al. Genomic variation landscape of the human gut microbiome Nature 493 2013 45 50
42. J.F. Nijkamp, M. Pop, and M.J. Reinders et al. Exploring variation-aware contig graphs for (comparative) metagenomics using MaryGold Bioinformatics 29 2013 2826 2834
43. Howe AC, Jansson J, Malfatti SA, et al. Assembling large, complex environmental metagenomes. http://arxiv:1212.2832.
44. I. Sharon, M.J. Morowitz, and B.C. Thomas et al. Time series community genomics analysis reveals rapid shifts in bacterial species, strains, and phage during infant gut colonization Genome Res 23 2013 111 120
45. T. Namiki, T. Hachiya, and H. Tanaka et al. MetaVelvet: an extension of Velvet assembler to de novo metagenome assembly from short sequence reads Nucleic Acids Res 40 2012 e155
46. Y. Peng, H.C. Leung, and S.M. Yiu et al. Meta-IDBA: a de novo assembler for metagenomic data Bioinformatics 27 2011 i94 i101
47. A.L. Delcher, K.A. Bratke, and E.C. Powers et al. Identifying bacterial genes and endosymbiont DNA with Glimmer Bioinformatics 23 2007 673 679
48. J. Besemer, A. Lomsadze, and M. Borodovsky GeneMarkS: a self-training method for prediction of gene starts in microbial genomes. Implications for finding sequence motifs in regulatory regions Nucleic Acids Res 29 2001 2607 2618
49. S. Abubucker, N. Segata, and J. Goll et al. Metabolic reconstruction for metagenomic data and its application to the human microbiome PLoS Comput Biol 8 2012 e1002358
50. F. Meyer, D. Paarmann, and M. D'Souza et al. The metagenomics RAST server-a public resource for the automatic phylogenetic and functional analysis of metagenomes BMC Bioinformatics 9 2008 386
51. K.M. Konwar, N.W. Hanson, and A.P. Page et al. MetaPathways: a modular pipeline for constructing pathway/genome databases from environmental sequence information BMC Bioinformatics 14 2013 202
52. M. Kanehisa The KEGG database Novartis Foundation symposium 247 2002 91 101 discussion 101-103, 119-128, 244-252
53. R. Overbeek, T. Begley, and R.M. Butler et al. The subsystems approach to genome annotation and its use in the project to annotate 1000 genomes Nucleic Acids Res 33 2005 5691 5702
54. R. Caspi, T. Altman, and K. Dreher et al. The MetaCyc database of metabolic pathways and enzymes and the BioCyc collection of pathway/genome databases Nucleic Acids Res 40 2012 D742 D753
55. R.L. Tatusov, M.Y. Galperin, and D.A. Natale et al. The COG database: a tool for genome-scale analysis of protein functions and evolution Nucleic Acids Res 28 2000 33 36
56. S. Powell, D. Szklarczyk, and K. Trachana et al. eggNOG v3.0: orthologous groups covering 1133 organisms at 41 different taxonomic ranges Nucleic Acids Res 40 2012 D284 D289
57. B.L. Cantarel, P.M. Coutinho, and C. Rancurel et al. The Carbohydrate-Active EnZymes database (CAZy): an expert resource for glycogenomics Nucleic Acids Res 37 2009 D233 D238
58. X.C. Morgan, and C. Huttenhower Chapter 12: human microbiome analysis PLoS Comput Biol 8 2012 e1002808
59. C.A. Lozupone, and R. Knight Species divergence and the measurement of microbial diversity FEMS Microbiol Rev 32 2008 557 578
60. R.L. Chazdon, R.K. Colwell, and J.S. Denslow et al. Statistical methods for estimating species richness of woody regeneration in primary and secondary rain forests of NE Costa Rica F. Dallmeier, J.A. Comiskey, Forest biodiversity research, monitoring and modeling: conceptual background and Old World case studies 1998 Parthenon Publishing Paris 285 309
61. E.H. Simpson Measurement of diversity Nature 163 1949 688
62. A.F. Zuur Principal coordinate analysis and non-metric multidimensional scaling. Analysing ecological data 2007 Springer New York 259 264
63. S.M. Huse, Y. Ye, and Y. Zhou et al. A core human microbiome as viewed through 16S rRNA sequence clusters PLoS One 7 2012 e34242
64. X.C. Morgan, T.L. Tickle, and H. Sokol et al. Dysfunction of the intestinal microbiome in inflammatory bowel disease and treatment Genome Biol 13 2012 R79
65. J.R. White, N. Nagarajan, and M. Pop Statistical methods for detecting differentially abundant features in clinical metagenomic samples PLoS Comput Biol 5 2009 e1000352
66. D.H. Parks, and R.G. Beiko Identifying biologically relevant differences between metagenomic communities Bioinformatics 26 2010 715 721
67. J.N. Paulson, O.C. Stine, and H.C. Bravo et al. Differential abundance analysis for microbial marker-gene surveys Nat Methods 10 2013 1200 1202
68. M.J. Gosalbes, A. Durban, and M. Pignatelli et al. Metatranscriptomic approach to analyze the functional human gut microbiota PLoS One 6 2011 e17447
69. B.S. Samuel, and J.I. Gordon A humanized gnotobiotic mouse model of host-archaeal-bacterial mutualism Proc Natl Acad Sci U S A 103 2006 10011 10016
70. G. Giannoukos, D.M. Ciulla, and K. Huang et al. Efficient and robust RNA-seq process for cultured bacteria and complex community transcriptomes Genome Biol 13 2012 R23
71. Y. Shi, G.W. Tyson, and J.M. Eppley et al. Integrated metatranscriptomic and metagenomic analyses of stratified microbial assemblages in the open ocean ISME J 5 2011 999 1013
72. M.M. Leimena, J. Ramiro-Garcia, and M. Davids et al. A comprehensive metatranscriptome analysis pipeline and its validation using human small intestine microbiota datasets BMC Genomics 14 2013 530
73. C. Trapnell, A. Roberts, and L. Goff et al. Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks Nat Protoc 7 2012 562 578
74. A. Mandlik, J. Livny, and W.P. Robins et al. RNA-Seq-based monitoring of infection-linked changes in Vibrio cholerae gene expression Cell Host Microbe 10 2011 165 174
75. B. Langmead, and S.L. Salzberg Fast gapped-read alignment with Bowtie 2 Nat Methods 9 2012 357 359
76. N.C. Verberkmoes, A.L. Russell, and M. Shah et al. Shotgun metaproteomics of the human distal gut microbiota ISME J 3 2009 179 189
77. K. Rooijers, C. Kolmeder, and C. Juste et al. An iterative workflow for mining the human intestinal metaproteome BMC Genomics 12 2011 6
78. H. Sokol, P. Seksik, and L. Rigottier-Gois et al. Specificities of the fecal microbiota in inflammatory bowel disease Inflamm Bowel Dis 12 2006 106 111
79. S. Kang, S.E. Denman, and M. Morrison et al. Dysbiosis of fecal microbiota in Crohn's disease patients as revealed by a custom phylogenetic microarray Inflamm Bowel Dis 16 2010 2034 2042
80. A.R. Erickson, B.L. Cantarel, and R. Lamendella et al. Integrated metagenomics/metaproteomics reveals human host-microbiota signatures of Crohn's disease PLoS One 7 2012 e49138
81. L.C. Antunes, J. Han, and R.B. Ferreira et al. Effect of antibiotic treatment on the intestinal metabolome Antimicrob Agents Chemother 55 2011 1494 1503
82. Z. Wang, E. Klipfell, and B.J. Bennett et al. Gut flora metabolism of phosphatidylcholine promotes cardiovascular disease Nature 472 2011 57 63
83. P.M. Smith, M.R. Howitt, and N. Panikov et al. The microbial metabolites, short-chain fatty acids, regulate colonic Treg cell homeostasis Science 341 2013 569 573
84. J. Pett-Ridge, and P.K. Weber NanoSIP: NanoSIMS applications for microbial biology Methods Mol Biol 881 2012 375 408
85. D. Berry, B. Stecher, and A. Schintlmeister et al. Host-compound foraging by intestinal microbiota revealed by single-cell stable isotope probing Proc Natl Acad Sci U S A 110 2013 4720 4725
86. L.A. McDonnell, and R.M. Heeren Imaging mass spectrometry Mass Spectrom Rev 26 2007 606 643
87. P. Hu, S.C. Janga, and M. Babu et al. Global functional atlas of Escherichia coli encompassing previously uncharacterized proteins PLoS Biol 7 2009 e96
88. F. Valour, S. Boisset, and L. Lebras et al. Clostridium sordellii brain abscess diagnosed by 16S rRNA gene sequencing J Clin Microbiol 48 2010 3443 3444
89. A.N. Flynn, C.A. Lyndon, and D.L. Church Identification by 16S rRNA gene sequencing of an Actinomyces hongkongensis isolate recovered from a patient with pelvic actinomycosis J Clin Microbiol 51 2013 2721 2723
90. C.S. Chin, J. Sorenson, and J.B. Harris et al. The origin of the Haitian cholera outbreak strain N Engl J Med 364 2011 33 42
91. N.A. Hasan, S.Y. Choi, and M. Eppinger et al. Genomic diversity of 2010 Haitian cholera outbreak strains Proc Natl Acad Sci U S A 109 2012 E2010 E2017
92. R. Schlaberg, K.E. Simmon, and M.A. Fisher A systematic approach for discovering novel, clinically relevant bacteria Emerg Infect Dis 18 2012 422 430
93. H.J. Haiser, D.B. Gootenberg, and K. Chatman et al. Predicting and manipulating cardiac drug inactivation by the human gut bacterium Eggerthella lenta Science 341 2013 295 298
94. B.D. Wallace, H. Wang, and K.T. Lane et al. Alleviating cancer drug toxicity by inhibiting a bacterial enzyme Science 330 2010 831 835
95. BioBakery. Available: http://huttenhower.sph.harvard.edu/biobakery. Accessed March 20, 2014.
96. J. Kuczynski, C.L. Lauber, and W.A. Walters et al. Experimental and analytical tools for studying the human microbiome Nat Rev Genet 13 2012 47 58
97. G. Henderson, F. Cox, and S. Kittelmann et al. Effect of DNA extraction methods and sampling techniques on the apparent structure of cow and sheep rumen microbial communities PLoS One 8 2013 e74787
98. A.M. Borman, M. Palmer, and E.M. Johnson Rapid methods for the extraction and archiving of molecular grade fungal genomic DNA Methods Mol Biol 968 2013 55 62
99. R.V. Thurber, M. Haynes, and M. Breitbart et al. Laboratory procedures to generate viral metagenomes Nat Protoc 4 2009 470 483
100. J. Walter, and R. Ley The human gut microbiome: ecology and recent evolutionary changes Ann Rev Microbiol 65 2011 411 429
101. F. Sommer, and F. Backhed The gut microbiota-masters of host development and physiology Nat Rev Microbiol 11 2013 227 238
102. J.C. Stearns, M.D. Lynch, and D.B. Senadheera et al. Bacterial biogeography of the human digestive tract Sci Rep 1 2011 170
103. D. Aguirre de Carcer, P.O. Cuiv, and T. Wang et al. Numerical ecology validates a biogeographical distribution and gender-based effect on mucosa-associated bacteria along the human colon ISME J 5 2011 801 809
104. T. Kuehbacher, A. Rehman, and P. Lepage et al. Intestinal TM7 bacterial phylogenies in active inflammatory bowel disease J Med Microbiol 57 2008 1569 1576
105. D.A. Cecchini, E. Laville, and S. Laguerre et al. Functional metagenomics reveals novel pathways of prebiotic breakdown by human gut bacteria PLoS One 8 2013 e72766
106. M. Baumgart, B. Dogan, and M. Rishniw et al. Culture independent analysis of ileal mucosa reveals a selective increase in invasive Escherichia coli of novel phylogeny relative to depletion of Clostridiales in Crohn's disease involving the ileum ISME J 1 2007 403 418
107. I. McHardy, M. Goudarzi, and M. Tong et al. Integrative analysis of the microbiome and metabolome of the human intestinal mucosal surface reveals exquisite inter-relationships Microbiome 1 2013 17
108. S. Sun, J. Chen, and W. Li et al. Community cyberinfrastructure for advanced microbial ecology research and analysis: the CAMERA resource Nucleic Acids Res 39 2011 D546 D551
109. D. Blankenberg, G. Von Kuster, and N. Coraor et al. Galaxy: a web-based genome analysis tool for experimentalists Curr Protoc Mol Biol 2010 Chapter 19:Unit 19.10.1-21
110. V.M. Markowitz, I.M. Chen, and K. Chu et al. IMG/M: the integrated metagenome data management and comparative analysis system Nucleic Acids Res 40 2012 D123 D129
111. D.H. Huson, A.F. Auch, and J. Qi et al. MEGAN analysis of metagenomic data Genome Res 17 2007 377 386
112. J. Goll, D.B. Rusch, and D.M. Tanenbaum et al. METAREP: JCVI metagenomics reports-an open source tool for high-performance comparative metagenomics Bioinformatics 26 2010 2631 2632
113. M. Arumugam, E.D. Harrington, and K.U. Foerstner et al. SmashCommunity: a metagenomic annotation and analysis tool Bioinformatics 26 2010 2977 2978
114. S.M. Huse, Welch D.B. Mark, and A. Voorhis et al. VAMPS: a website for visualization and analysis of microbial population structures BMC Bioinformatics 15 2014 41