Student or educator? Sign up with your school email and get 6 months of Pro free.
Cited by 326

The DOI matches its Crossref record; 28 of the 28 references it cites were found in a registry or an index.

Computational meta'omics for microbial community studies

Open access
Segata, Nicola, Boernigen, Daniela, Tickle, Timothy L, Morgan, Xochitl C, Garrett, Wendy S, Huttenhower, Curtis·2013·Molecular Systems Biology

Abstract

Complex microbial communities are an integral part of the Earth's ecosystem and of our bodies in health and disease. In the last two decades, culture‐independent approaches have provided new insights into their structure and function, with the exponentially decreasing cost of high‐throughput sequencing resulting in broadly available tools for microbial surveys. However, the field remains far from reaching a technological plateau, as both computational techniques and nucleotide sequencing platforms for microbial genomic and transcriptional content continue to improve. Current microbiome analyses are thus starting to adopt multiple and complementary meta'omic approaches, leading to unprecedented opportunities to comprehensively and accurately characterize microbial communities and their interactions with their environments and hosts. This diversity of available assays, analysis methods, and public data is in turn beginning to enable microbiome‐based predictive and modeling tools. We thus review here the technological and computational meta'omics approaches that are already available, those that are under active development, their success in biological discovery, and several outstanding challenges.

Overview

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1038/msb.2013.22

Cites

28 of 28 references verified0 citation errors · 0 not checkable

Statistics

Verification

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Citations

Cites

Show all 28 references

Research works printed but not linked: 147

  1. Abubucker S, Segata N, Goll J, Schubert AM, Izard J, Cantarel BL, Rodriguez‐Mueller B, Zucker J, Thiagarajan M, Henrissat B, White O, Kelley ST, Methe B, Schloss PD, Gevers D, Mitreva M, Huttenhower C (2012) Metabolic reconstruction for metagenomic data and its application to the human microbiome. PLoS Comput Biol 8: e1002358 · DOI · Paper page
  2. Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI‐BLAST: a new generation of protein database search programs. Nucleic Acids Res 25: 3389–3402 · DOI · Paper page
  3. Arumugam M, Harrington ED, Foerstner KU, Raes J, Bork P (2010) SmashCommunity: a metagenomic annotation and analysis tool. Bioinformatics 26: 2977–2978 · DOI
  4. Bartram AK, Lynch MDJ, Stearns JC, Moreno‐Hagelsieb G, Neufeld JD (2011) Generation of multimillion‐sequence 16S rRNA gene libraries from complex microbial communities by assembling paired‐end Illumina reads. Appl Environ Microbiol 77: 3846–3852 · DOI · Paper page
  5. Berger SA, Stamatakis A (2011) Aligning short reads to reference alignments and trees. Bioinformatics 27: 2068–2075 · DOI · Paper page
  6. Bidle KD, Vardi A (2011) A chemical arms race at sea mediates algal host‐virus interactions. Curr Opin Microbiol 14: 449–457 · DOI
  7. Bittner L, Halary S, Payri C, Cruaud C, de Reviers B, Lopez P, Bapteste E (2010) Some considerations for analyzing biodiversity using integrative metagenomics and gene networks. Biol Direct 5: 47 · DOI
  8. Blainey PC, Mosier AC, Potanina A, Francis CA, Quake SR (2011) Genome of a low‐salinity ammonia‐oxidizing archaeon determined by single‐cell and metagenomic analysis. PLoS One 6: e16626 · DOI · Paper page
  9. Brady A, Salzberg S (2011) PhymmBL expanded: confidence scores, custom databases, parallelization and more. Nat Methods 8: 367 · DOI
  10. Bucci V, Bradde S, Biroli G, Xavier JB (2012) Social interaction, noise and antibiotic‐mediated switches in the intestinal microbiota. PLoS Comput Biol 8: e1002497 · DOI
  11. Caporaso JG, Lauber CL, Walters WA, Berg‐Lyons D, Huntley J, Fierer N, Owens SM, Betley J, Fraser L, Bauer M (2012) Ultra‐high‐throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms. ISME J 6: 1621–1624 · DOI · Paper page
  12. Chaffron S, Rehrauer H, Pernthaler J, von Mering C (2010) A global network of coexisting microbes from environmental and whole‐genome sequence data. Genome Res 20: 947–959 · DOI · Paper page
  13. Chen J, Bittinger K, Charlson ES, Hoffmann C, Lewis J, Wu GD, Collman RG, Bushman FD, Li H (2012) Associating microbiome composition with environmental covariates using generalized UniFrac distances. Bioinformatics 28: 2106–2113 · DOI · Paper page
  14. Chen J, Novick RP (2009) Phage‐mediated intergeneric transfer of toxin genes. Science 323: 139–141 · DOI · Paper page
  15. Croucher NJ, Harris SR, Fraser C, Quail MA, Burton J, van der Linden M, McGee L, von Gottberg A, Song JH, Ko KS (2011) Rapid pneumococcal evolution in response to clinical interventions. Science 331: 430–434 · DOI · Paper page
  16. Croxen MA, Finlay BB (2009) Molecular mechanisms of Escherichia coli pathogenicity. Nat Rev Microbiol 8: 26–38 · DOI · Paper page
  17. Culley AI, Lang AS, Suttle CA (2006) Metagenomic analysis of coastal RNA virus communities. Science 312: 1795–1798 · DOI · Paper page
  18. DeLong EF, Pace NR (2001) Environmental diversity of bacteria and archaea. Syst Biol 50: 470–478 · DOI
  19. Dethlefsen L, Relman DA (2011) Incomplete recovery and individualized responses of the human distal gut microbiota to repeated antibiotic perturbation. Proc Natl Acad Sci 108: 4554–4561 · DOI · Paper page
  20. Dewhirst FE, Chien CC, Paster BJ, Ericson RL, Orcutt RP, Schauer DB, Fox JG (1999) Phylogeny of the defined murine microbiota: altered Schaedler flora. Appl Environ Microbiol 65: 3287–3292 · DOI · Paper page
  21. Diaz NN, Krause L, Goesmann A, Niehaus K, Nattkemper TW (2009) TACOA–Taxonomic classification of environmental genomic fragments using a kernelized nearest neighbor approach. BMC Bioinformatics 10: 56 · DOI
  22. Dollive S, Peterfreund GL, Sherrill‐Mix S, Bittinger K, Sinha R, Hoffmann C, Nabel C, Hill DA, Artis D, Bachman MA (2012) A tool kit for quantifying eukaryotic rRNA gene sequences from human microbiome samples. Genome Biol 13: R60 · DOI · Paper page
  23. Dominguez‐Bello MG, Costello EK, Contreras M, Magris M, Hidalgo G, Fierer N, Knight R (2010) Delivery mode shapes the acquisition and structure of the initial microbiota across multiple body habitats in newborns. Proc Natl Acad Sci 107: 11971–11975 · DOI · Paper page
  24. Edgar RC (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26: 2460–2461 · DOI · Paper page
  25. Faith JJ, McNulty NP, Rey FE, Gordon JI (2011) Predicting a human gut microbiota's response to diet in gnotobiotic mice. Science 333: 101–104 · DOI · Paper page
  26. Fodor AA, DeSantis TZ, Wylie KM, Badger JH, Ye Y, Hepburn T, Hu P, Sodergren E, Liolios K, Huot‐Creasy H, Birren BW, Earl AM (2012) The ‘most wanted’ taxa from the human microbiome for whole genome sequencing. PLoS One 7: e41294 · DOI
  27. Frias‐Lopez J, Shi Y, Tyson GW, Coleman ML, Schuster SC, Chisholm SW, Delong EF (2008) Microbial community gene expression in ocean surface waters. Proc Natl Acad Sci USA 105: 3805–3810 · DOI · Paper page
  28. Friedman J, Alm EJ (2012) Inferring correlation networks from genomic survey data. PLoS Comput Biol 8: e1002687 · DOI · Paper page
  29. Gajer P, Brotman RM, Bai G, Sakamoto J, Schütte UM, Zhong X, Koenig SS, Fu L, Ma ZS, Zhou X (2012) Temporal dynamics of the human vaginal microbiota. Sci Transl Med 4: 132ra152 · DOI · Paper page
  30. Garrett WS, Gallini CA, Yatsunenko T, Michaud M, DuBois A, Delaney ML, Punit S, Karlsson M, Bry L, Glickman JN, Gordon JI, Onderdonk AB, Glimcher LH (2010) Enterobacteriaceae act in concert with the gut microbiota to induce spontaneous and maternally transmitted colitis. Cell Host Microbe 8: 292–300 · DOI · Paper page
  31. Gerlach W, Stoye J (2011) Taxonomic classification of metagenomic shotgun sequences with CARMA3. Nucleic Acids Res 39: e91–e91 · DOI
  32. Ghosh T, Haque M, Mande S (2010) DiScRIBinATE: a rapid method for accurate taxonomic classification of metagenomic sequences. BMC Bioinformatics 11: S14 · DOI
  33. Giannakis M, Chen SL, Karam SM, Engstrand L, Gordon JI (2008) Helicobacter pylori evolution during progression from chronic atrophic gastritis to gastric cancer and its impact on gastric stem cells. Proc Natl Acad Sci 105: 4358–4363 · DOI
  34. Gilbert JA, Hughes M (2011) Gene expression profiling: metatranscriptomics. Methods in molecular biology (Clifton, NJ) 733: 195–205 · DOI
  35. Goll J, Rusch DB, Tanenbaum DM, Thiagarajan M, Li K, Methé BA, Yooseph S (2010) METAREP: JCVI metagenomics reports—an open source tool for high‐performance comparative metagenomics. Bioinformatics 26: 2631–2632 · DOI
  36. Goodman AL, Kallstrom G, Faith JJ, Reyes A, Moore A, Dantas G, Gordon JI (2011) Extensive personal human gut microbiota culture collections characterized and manipulated in gnotobiotic mice. Proc Natl Acad Sci 108: 6252–6257 · DOI · Paper page
  37. Gori F, Folino G, Jetten MSM, Marchiori E (2011) MTR: taxonomic annotation of short metagenomic reads using clustering at multiple taxonomic ranks. Bioinformatics 27: 196–203 · DOI
  38. Gosalbes MJ, Durban A, Pignatelli M, Abellan JJ, Jimenez‐Hernandez N, Perez‐Cobas AE, Latorre A, Moya A (2011) Metatranscriptomic approach to analyze the functional human gut microbiota. PLoS One 6: e17447 · DOI · Paper page
  39. Hakoyama T, Niimi K, Watanabe H, Tabata R, Matsubara J, Sato S, Nakamura Y, Tabata S, Jichun L, Matsumoto T (2009) Host plant genome overcomes the lack of a bacterial gene for symbiotic nitrogen fixation. Nature 462: 514–517 · doi:10.1038/nature08594
  40. Harrington ED, Arumugam M, Raes J, Bork P, Relman DA (2010) SmashCell: a software framework for the analysis of single‐cell amplified genome sequences. Bioinformatics 26: 2979–2980 · doi:10.1093/bioinformatics/btq564
  41. Hess M, Sczyrba A, Egan R, Kim TW, Chokhawala H, Schroth G, Luo S, Clark DS, Chen F, Zhang T (2011) Metagenomic discovery of biomass‐degrading genes and genomes from cow rumen. Science 331: 463–467 · DOI · Paper page
  42. Hooper LV, Littman DR, Macpherson AJ (2012) Interactions between the microbiota and the immune system. Science 336: 1268–1273 · DOI · Paper page
  43. Horton M, Bodenhausen N, Bergelson J (2010) MARTA: a suite of Java‐based tools for assigning taxonomic status to DNA sequences. Bioinformatics 26: 568–569 · DOI
  44. Hughes TR, Marton MJ, Jones AR, Roberts CJ, Stoughton R, Armour CD, Bennett HA, Coffey E, Dai H, He YD (2000) Functional discovery via a compendium of expression profiles. Cell 102: 109–126 · DOI · Paper page
  45. Huse SM, Dethlefsen L, Huber JA, Welch DM, Relman DA, Sogin ML (2008) Exploring microbial diversity and taxonomy using SSU rRNA hypervariable tag sequencing. PLoS Genet 4: e1000255 · DOI · Paper page
  46. Huson DH, Auch AF, Qi J, Schuster SC (2007) MEGAN analysis of metagenomic data. Genome Res 17: 377–386 · DOI · Paper page
  47. Hyland C, Pinney JW, McConkey GA, Westhead DR (2006) metaSHARK: a WWW platform for interactive exploration of metabolic networks. Nucleic Acids Res 34: W725–W728 · DOI
  48. Ivanov II, Atarashi K, Manel N, Brodie EL, Shima T, Karaoz U, Wei D, Goldfarb KC, Santee CA, Lynch SV, Tanoue T, Imaoka A, Itoh K, Takeda K, Umesaki Y, Honda K, Littman DR (2009) Induction of intestinal Th17 cells by segmented filamentous bacteria. Cell 139: 485–498 · DOI · Paper page
  49. Jansson J, Willing B, Lucio M, Fekete A, Dicksved J, Halfvarson J, Tysk C, Schmitt‐Kopplin P (2009) Metabolomics reveals metabolic biomarkers of Crohn's disease. PloS One 4: e6386 · DOI · Paper page
  50. Kamada N, Kim YG, Sham HP, Vallance BA, Puente JL, Martens EC, Nunez G (2012) Regulated virulence controls the ability of a pathogen to compete with the gut microbiota. Science 336: 1325–1329 · DOI · Paper page
  51. Kanehisa M, Goto S (2000) KEGG: kyoto encyclopedia of genes and genomes. Nucleic Acids Res 28: 27–30 · DOI · Paper page
  52. Kinross JM, Darzi AW, Nicholson JK (2011) Gut microbiome‐host interactions in health and disease. Genome Med 3: 14 · DOI · Paper page
  53. Klitgord N, Segrè D (2010) Environments that induce synthetic microbial ecosystems. PLoS Comput Biol 6: e1001002 · DOI · Paper page
  54. Knights D, Kuczynski J, Charlson ES, Zaneveld J, Mozer MC, Collman RG, Bushman FD, Knight R, Kelley ST (2011) Bayesian community‐wide culture‐independent microbial source tracking. Nat Methods 8: 761–763 · DOI · Paper page
  55. Konopka A (2009) What is microbial community ecology? ISME J 3: 1223–1230 · DOI · Paper page
  56. Kostic AD, Gevers D, Pedamallu CS, Michaud M, Duke F, Earl AM, Ojesina AI, Jung J, Bass AJ, Tabernero J, Baselga J, Liu C, Shivdasani RA, Ogino S, Birren BW, Huttenhower C, Garrett WS, Meyerson M (2012) Genomic analysis identifies association of Fusobacterium with colorectal carcinoma. Genome Res 22: 292–298 · DOI · Paper page
  57. Kristiansson E, Hugenholtz P, Dalevi D (2009) ShotgunFunctionalizeR: an R‐package for functional comparison of metagenomes. Bioinformatics 25: 2737–2738 · DOI
  58. Kultima JR, Sunagawa S, Li J, Chen W, Chen H, Mende DR, Arumugam M, Pan Q, Liu B, Qin J (2012) MOCAT: a metagenomics assembly and gene prediction toolkit. PloS One 7: e47656 · DOI · Paper page
  59. Kvist T, Ahring BK, Lasken RS, Westermann P (2007) Specific single‐cell isolation and genomic amplification of uncultured microorganisms. Appl Microbiol Biotechnol 74: 926–935 · DOI
  60. Langmead B, Salzberg SL (2012) Fast gapped‐read alignment with Bowtie 2. Nat Methods 9: 357–359 · DOI · Paper page
  61. Larsen PE, Collart FR, Field D, Meyer F, Keegan KP, Henry CS, McGrath J, Quinn J, Gilbert JA (2011) Predicted Relative Metabolomic Turnover (PRMT): determining metabolic turnover from a coastal marine metagenomic dataset. Microbial Inform Exper 1: 4 · DOI
  62. Larsen PE, Field D, Gilbert JA (2012) Predicting bacterial community assemblages using an artificial neural network approach. Nat Methods 9: 621–625 · DOI · Paper page
  63. Laserson J, Jojic V, Koller D (2011) Genovo: de novo assembly for metagenomes. J Comput Biol 18: 429–443 · DOI
  64. Lasken RS (2012) Genomic sequencing of uncultured microorganisms from single cells. Nat Rev Microbiol 10: 631–640 · DOI · Paper page
  65. Lefébure T, Stanhope MJ (2007) Evolution of the core and pan‐genome of Streptococcus: positive selection, recombination, and genome composition. Genome Biol 8: R71 · DOI · Paper page
  66. Ley RE, Lozupone CA, Hamady M, Knight R, Gordon JI (2008) Worlds within worlds: evolution of the vertebrate gut microbiota. Nat Rev Microbiol 6: 776–788 · DOI · Paper page
  67. Li H, Durbin R (2010) Fast and accurate long‐read alignment with Burrows‐Wheeler transform. Bioinformatics 26: 589–595 · DOI · Paper page
  68. Li M, Wang B, Zhang M, Rantalainen M, Wang S, Zhou H, Zhang Y, Shen J, Pang X, Zhang M, Wei H, Chen Y, Lu H, Zuo J, Su M, Qiu Y, Jia W, Xiao C, Smith LM, Yang S et al (2008) Symbiotic gut microbes modulate human metabolic phenotypes. Proc Natl Acad Sci USA 105: 2117–2122 · DOI · Paper page
  69. Li W (2009) Analysis and comparison of very large metagenomes with fast clustering and functional annotation. BMC Bioinformatics 10: 359 · DOI
  70. Li X, LeBlanc J, Truong A, Vuthoori R, Chen SS, Lustgarten JL, Roth B, Allard J, Ippoliti A, Presley LL, Borneman J, Bigbee WL, Gopalakrishnan V, Graeber TG, Elashoff D, Braun J, Goodglick L (2011) A metaproteomic approach to study human‐microbial ecosystems at the mucosal luminal interface. PloS One 6: e26542 · DOI
  71. Lieberman TD, Michel JB, Aingaran M, Potter‐Bynoe G, Roux D, Davis MR Jr, Skurnik D, Leiby N, LiPuma JJ, Goldberg JB (2011) Parallel bacterial evolution within multiple patients identifies candidate pathogenicity genes. Nat Genet 43: 1275–1280 · DOI · Paper page
  72. Lim YW, Schmieder R, Haynes M, Willner D, Furlan M, Youle M, Abbott K, Edwards R, Evangelista J, Conrad D (2012) Metagenomics and metatranscriptomics: Windows on CF‐associated viral and microbial communities. J Cyst Fibros 12: 154–164 · DOI · Paper page
  73. Liu B, Gibbons T, Ghodsi M, Treangen T, Pop M (2011) Accurate and fast estimation of taxonomic profiles from metagenomic shotgun sequences. BMC Genomics 12: Suppl 2 S4 · DOI
  74. Lovell D, Muller W, Taylor J, Zwart A, Helliwell C (2010) Caution! Compositions!. Report Number: EP10994. CSIRO Mathematical and Information Sciences
  75. Lozupone C, Faust K, Raes J, Faith JJ, Frank DN, Zaneveld J, Gordon JI, Knight R (2012) Identifying genomic and metabolic features that can underlie early successional and opportunistic lifestyles of human gut symbionts. Genome Res 22: 1974–1984 · DOI
  76. Luo C, Tsementzi D, Kyrpides N, Read T, Konstantinidis KT (2012) Direct comparisons of Illumina vs. Roche 454 sequencing technologies on the same microbial community DNA sample. PLoS One 7: e30087 · DOI · Paper page
  77. Marcy Y, Ouverney C, Bik EM, Losekann T, Ivanova N, Martin HG, Szeto E, Platt D, Hugenholtz P, Relman DA, Quake SR (2007) Dissecting biological ‘dark matter’ with single‐cell genetic analysis of rare and uncultivated TM7 microbes from the human mouth. Proc Natl Acad Sci USA 104: 11889–11894 · DOI · Paper page
  78. Markowitz VM, Chen IM, Palaniappan K, Chu K, Szeto E, Grechkin Y, Ratner A, Jacob B, Huang J, Williams P, Huntemann M, Anderson I, Mavromatis K, Ivanova NN, Kyrpides NC (2012a) IMG: the Integrated Microbial Genomes database and comparative analysis system. Nucleic Acids Res 40: D115–D122 · DOI · Paper page
  79. Markowitz VM, Chen IMA, Chu K, Szeto E, Palaniappan K, Grechkin Y, Ratner A, Jacob B, Pati A, Huntemann M (2012b) IMG/M: the integrated metagenome data management and comparative analysis system. Nucleic Acids Res 40: D123–D129 · DOI · Paper page
  80. Marsh P, Hunter J, Bowden G, Hamilton I, McKee A, Hardie J, Ellwood D (1983) The influence of growth rate and nutrient limitation on the microbial composition and biochemical properties of a mixed culture of oral bacteria grown in a chemostat. J Gen Microbiol 129: 755–770
  81. Mason OU, Hazen TC, Borglin S, Chain PS, Dubinsky EA, Fortney JL, Han J, Holman HY, Hultman J, Lamendella R, Mackelprang R, Malfatti S, Tom LM, Tringe SG, Woyke T, Zhou J, Rubin EM, Jansson JK (2012) Metagenome, metatranscriptome and single‐cell sequencing reveal microbial response to Deepwater Horizon oil spill. ISME J 6: 1715–1727 · DOI · Paper page
  82. McBain A, MacFarlane G (2001) Modulation of genotoxic enzyme activities by non‐digestible oligosaccharide metabolism in in‐vitro human gut bacterial ecosystems. J Med Microbiol 50: 833–842 · DOI
  83. McCarren J, Becker JW, Repeta DJ, Shi Y, Young CR, Malmstrom RR, Chisholm SW, DeLong EF (2010) Microbial community transcriptomes reveal microbes and metabolic pathways associated with dissolved organic matter turnover in the sea. Proc Natl Acad Sci 107: 16420–16427 · DOI · Paper page
  84. McDaniel LD, Young E, Delaney J, Ruhnau F, Ritchie KB, Paul JH (2010) High frequency of horizontal gene transfer in the oceans. Science 330: 50–50 · DOI · Paper page
  85. McElroy KE, Luciani F, Thomas T (2012) GemSIM: general, error‐model based simulator of next‐generation sequencing data. BMC Genomics 13: 74 · DOI · Paper page
  86. McFall‐Ngai M (2008) Host‐microbe symbiosis: the squid‐Vibrio association—a naturally occurring, experimental model of animal/bacterial partnerships. Adv Exp Med Biol 635: 102–112 · DOI
  87. McFall‐Ngai M, Heath‐Heckman EAC, Gillette AA, Peyer SM, Harvie EA (2011) The secret languages of coevolved symbioses: Insights from the Euprymna scolopes Vibrio fischeri symbiosis. Semin Immunol 24: 3–8 · DOI
  88. McNulty NP, Yatsunenko T, Hsiao A, Faith JJ, Muegge BD, Goodman AL, Henrissat B, Oozeer R, Cools‐Portier S, Gobert G (2011) The impact of a consortium of fermented milk strains on the gut microbiome of gnotobiotic mice and monozygotic twins. Sci Transl Med 3: 106ra106 · DOI · Paper page
  89. Mende DR, Waller AS, Sunagawa S, Jarvelin AI, Chan MM, Arumugam M, Raes J, Bork P (2012) Assessment of metagenomic assembly using simulated next generation sequencing data. PLoS One 7: e31386 · DOI · Paper page
  90. Meyer F, Paarmann D, D'Souza M, Olson R, Glass EM, Kubal M, Paczian T, Rodriguez A, Stevens R, Wilke A, Wilkening J, Edwards RA (2008) The metagenomics RAST server ‐ a public resource for the automatic phylogenetic and functional analysis of metagenomes. BMC Bioinformatics 9: 386 · DOI · Paper page
  91. Mitra S, Rupek P, Richter D, Urich T, Gilbert J, Meyer F, Wilke A, Huson D (2011) Functional analysis of metagenomes and metatranscriptomes using SEED and KEGG. BMC Bioinformatics 12: S21 · DOI
  92. Mohammed M, Ghosh T, Reddy R, Reddy CVSK, Singh N, Mande S (2011a) INDUS‐A composition based approach for rapid and accurate taxonomic classification of metagenomic sequences. BMC Genomics 12: S4 · DOI
  93. Mohammed MH, Ghosh TS, Singh NK, Mande SS (2011b) SPHINX—an algorithm for taxonomic binning of metagenomic sequences. Bioinformatics 27: 22–30 · DOI
  94. Monzoorul Haque M, Ghosh TS, Komanduri D, Mande SS (2009) SOrt‐ITEMS: Sequence orthology based approach for improved taxonomic estimation of metagenomic sequences. Bioinformatics 25: 1722–1730 · DOI
  95. Moran NA, McCutcheon JP, Nakabachi A (2008) Genomics and evolution of heritable bacterial symbionts. Annu Rev Genet 42: 165–190 · DOI · Paper page
  96. Moran NA, Munson MA, Baumann P, Ishikawa H (1993) A molecular clock in endosymbiotic bacteria is calibrated using the insect hosts. Proc R Soc Lond Ser B Biol Sci 253: 167–171 · DOI · Paper page
  97. Morgan XC, Tickle TL, Sokol H, Gevers D, Devaney KL, Ward DV, Reyes JA, Shah SA, Leleiko N, Snapper SB, Bousvaros A, Korzenik J, Sands BE, Xavier RJ, Huttenhower C (2012) Dysfunction of the intestinal microbiome in inflammatory bowel disease and treatment. Genome Biol 13: R79 · DOI · Paper page
  98. Nalbantoglu OU, Way SF, Hinrichs SH, Sayood K (2011) RAIphy: Phylogenetic classification of metagenomics samples using iterative refinement of relative abundance index profiles. BMC Bioinformatics 12: 41 · DOI
  99. Namiki T, Hachiya T, Tanaka H, Sakakibara Y (2012) MetaVelvet: an extension of Velvet assembler to de novo metagenome assembly from short sequence reads. Nucleic Acids Res 40: e155 · DOI · Paper page
  100. Narasingarao P, Podell S, Ugalde JA, Brochier‐Armanet C, Emerson JB, Brocks JJ, Heidelberg KB, Banfield JF, Allen EE (2012) De novo metagenomic assembly reveals abundant novel major lineage of Archaea in hypersaline microbial communities. ISME J 6: 81–93 · DOI · Paper page
  101. Overbeek R, Begley T, Butler RM, Choudhuri JV, Chuang HY, Cohoon M, de Crécy‐Lagard V, Diaz N, Disz T, Edwards R (2005) The subsystems approach to genome annotation and its use in the project to annotate 1000 genomes. Nucleic Acids Res 33: 5691–5702 · DOI · Paper page
  102. Pamp SJ, Harrington ED, Quake SR, Relman DA, Blainey PC (2012) Single‐cell sequencing provides clues about the host interactions of segmented filamentous bacteria (SFB). Genome Res 22: 1107–1119 · DOI
  103. Parks DH, Beiko RG (2010) Identifying biologically relevant differences between metagenomic communities. Bioinformatics 26: 715–721 · DOI · Paper page
  104. Parks DH, MacDonald NJ, Beiko RG (2011) Classifying short genomic fragments from novel lineages using composition and homology. BMC Bioinformatics 12: 328 · DOI
  105. Pati A, Heath LS, Kyrpides NC, Ivanova N (2011) ClaMS: a classifier for metagenomic sequences. Stand Genomic Sci 5: 248 · DOI
  106. Patil KR, Haider P, Pope PB, Turnbaugh PJ, Morrison M, Scheffer T, McHardy AC (2011) Taxonomic metagenome sequence assignment with structured output models. Nat Methods 8: 191–192 · DOI
  107. Patil KR, Roune L, McHardy AC (2012) The PhyloPythiaS Web Server for Taxonomic Assignment of Metagenome Sequences. PloS One 7: e38581 · DOI
  108. Pell J, Hintze A, Canino‐Koning R, Howe A, Tiedje JM, Brown CT (2012) Scaling metagenome sequence assembly with probabilistic de Bruijn graphs. Proc Natl Acad Sci USA 109: 13272–13277 · DOI · Paper page
  109. Peng Y, Leung HC, Yiu SM, Chin FY (2011) Meta‐IDBA: a de Novo assembler for metagenomic data. Bioinformatics 27: i94–101 · DOI · Paper page
  110. Peng Y, Leung HC, Yiu SM, Chin FY (2012) IDBA‐UD: a de novo assembler for single‐cell and metagenomic sequencing data with highly uneven depth. Bioinformatics 28: 1420–1428 · DOI · Paper page
  111. Pignatelli M, Moya A (2011) Evaluating the fidelity of de novo short read metagenomic assembly using simulated data. PLoS One 6: e19984 · DOI
  112. Powell S, Szklarczyk D, Trachana K, Roth A, Kuhn M, Muller J, Arnold R, Rattei T, Letunic I, Doerks T (2012) eggNOG v3. 0: orthologous groups covering 1133 organisms at 41 different taxonomic ranges. Nucleic Acids Res 40: D284–D289 · DOI · Paper page
  113. Punta M, Coggill PC, Eberhardt RY, Mistry J, Tate J, Boursnell C, Pang N, Forslund K, Ceric G, Clements J, Heger A, Holm L, Sonnhammer EL, Eddy SR, Bateman A, Finn RD (2012) The Pfam protein families database. Nucleic Acids Res 40: D290–D301 · DOI · Paper page
  114. Raes J, Letunic I, Yamada T, Jensen LJ, Bork P (2011) Toward molecular trait‐based ecology through integration of biogeochemical, geographical and metagenomic data. Mol Syst Biol 7: 473 · DOI · Paper page
  115. Richter DC, Ott F, Auch AF, Schmid R, Huson DH (2008) MetaSim—A sequencing simulator for genomics and metagenomics. PloS One 3: e3373 · DOI · Paper page
  116. Rocap G, Larimer FW, Lamerdin J, Malfatti S, Chain P, Ahlgren NA, Arellano A, Coleman M, Hauser L, Hess WR, Johnson ZI, Land M, Lindell D, Post AF, Regala W, Shah M, Shaw SL, Steglich C, Sullivan MB, Ting CS et al (2003) Genome divergence in two Prochlorococcus ecotypes reflects oceanic niche differentiation. Nature 424: 1042–1047 · DOI · Paper page
  117. Rosen GL, Reichenberger ER, Rosenfeld AM (2011) NBC: the Naive Bayes Classification tool webserver for taxonomic classification of metagenomic reads. Bioinformatics 27: 127–129 · DOI · Paper page
  118. Schmidt TM, DeLong EF, Pace NR (1991) Analysis of a marine picoplankton community by 16S rRNA gene cloning and sequencing. J Bacteriol 173: 4371–4378 · DOI · Paper page
  119. Schreiber F, Gumrich P, Daniel R, Meinicke P (2010) Treephyler: fast taxonomic profiling of metagenomes. Bioinformatics 26: 960–961 · DOI
  120. Schultz J, Milpetz F, Bork P, Ponting CP (1998) SMART, a simple modular architecture research tool: identification of signaling domains. Proc Natl Acad Sci 95: 5857–5864 · DOI · Paper page
  121. Sczesnak A, Segata N, Qin X, Gevers D, Petrosino JF, Huttenhower C, Littman DR, Ivanov II (2011) The genome of th17 cell‐inducing segmented filamentous bacteria reveals extensive auxotrophy and adaptations to the intestinal environment. Cell Host Microbe 10: 260–272 · DOI
  122. Segata N, Izard J, Waldron L, Gevers D, Miropolsky L, Garrett WS, Huttenhower C (2011) Metagenomic biomarker discovery and explanation. Genome Biol 12: R60 · DOI · Paper page
  123. Seshadri R, Kravitz SA, Smarr L, Gilna P, Frazier M (2007) CAMERA: a community resource for metagenomics. PLoS Biol 5: e75 · DOI · Paper page
  124. Shi Y, Tyson GW, DeLong EF (2009) Metatranscriptomics reveals unique microbial small RNAs in the ocean's water column. Nature 459: 266–269 · DOI · Paper page
  125. Shi Y, Tyson GW, Eppley JM, DeLong EF (2011) Integrated metatranscriptomic and metagenomic analyses of stratified microbial assemblages in the open ocean. ISME J 5: 999–1013 · DOI · Paper page
  126. Smillie CS, Smith MB, Friedman J, Cordero OX, David LA, Alm EJ (2011) Ecology drives a global network of gene exchange connecting the human microbiome. Nature 480: 241–244 · DOI · Paper page
  127. Southward AJ, Langmead O, Hardman‐Mountford NJ, Aiken J, Boalch GT, Dando PR, Genner MJ, Joint I, Kendall MA, Halliday NC, Harris RP, Leaper R, Mieszkowska N, Pingree RD, Richardson AJ, Sims DW, Smith T, Walne AW, Hawkins SJ (2005) Long‐term oceanographic and ecological research in the Western English Channel. Adv Marine Biol 47: 1–105
  128. Su CH, Hsu MT, Chiang S, Cheng JH, Weng FC, Wang D, Tsai HK (2011) MetaABC—an integrated metagenomics platform for data adjustment, binning and clustering. Bioinformatics 27: 2298–2299 · doi:10.1093/bioinformatics/btr376
  129. Tatusov RL, Koonin EV, Lipman DJ (1997) A genomic perspective on protein families. Science 278: 631–637 · DOI · Paper page
  130. Teeling H, Waldmann J, Lombardot T, Bauer M, Glöckner FO (2004) TETRA: a web‐service and a stand‐alone program for the analysis and comparison of tetranucleotide usage patterns in DNA sequences. BMC Bioinformatics 5: 163 · DOI · Paper page
  131. Treangen TJ, Koren S, Astrovskaya I, Sommer D, Liu B, Pop M (2011a) MetAMOS: a metagenomic assembly and analysis pipeline for AMOS. Genome Biol 12: 1–27 · doi:10.1186/1465-6906-12-s1-p25
  132. Treangen TJ, Sommer DD, Angly FE, Koren S, Pop M (2011b) Next generation sequence assembly with AMOS. Curr Protoc Bioinformatics 33: 11.8.1–11.8.18 · DOI · Paper page
  133. Tringe SG, Hugenholtz P (2008) A renaissance for the pioneering 16S rRNA gene. Curr Opin Microbiol 11: 442–446 · DOI · Paper page
  134. Turnbaugh PJ, Gordon JI (2008) An invitation to the marriage of metagenomics and metabolomics. Cell 134: 708–713 · DOI · Paper page
  135. Turnbaugh PJ, Hamady M, Yatsunenko T, Cantarel BL, Duncan A, Ley RE, Sogin ML, Jones WJ, Roe BA, Affourtit JP, Egholm M, Henrissat B, Heath AC, Knight R, Gordon JI (2009a) A core gut microbiome in obese and lean twins. Nature 457: 480–484 · DOI · Paper page
  136. Turnbaugh PJ, Quince C, Faith JJ, McHardy AC, Yatsunenko T, Niazi F, Affourtit J, Egholm M, Henrissat B, Knight R, Gordon JI (2010) Organismal, genetic, and transcriptional variation in the deeply sequenced gut microbiomes of identical twins. Proc Natl Acad Sci USA 107: 7503–7508 · DOI · Paper page
  137. Verberkmoes NC, Russell AL, Shah M, Godzik A, Rosenquist M, Halfvarson J, Lefsrud MG, Apajalahti J, Tysk C, Hettich RL, Jansson JK (2009) Shotgun metaproteomics of the human distal gut microbiota. ISME J 3: 179–189 · DOI · Paper page
  138. Wang Y, Leung HCM, Yiu S, Chin FYL (2012) MetaCluster 4.0: a novel binning algorithm for NGS reads and huge number of species. Journal of Computational Biology 19: 241–249 · DOI
  139. Weber M, Teeling H, Huang S, Waldmann J, Kassabgy M, Fuchs BM, Klindworth A, Klockow C, Wichels A, Gerdts G (2010) Practical application of self‐organizing maps to interrelate biodiversity and functional data in NGS‐based metagenomics. ISME J 5: 918–928 · DOI
  140. White JR, Nagarajan N, Pop M (2009) Statistical methods for detecting differentially abundant features in clinical metagenomic samples. PLoS Comput Biol 5: e1000352 · DOI · Paper page
  141. Wilmes P, Bond PL (2006) Metaproteomics: studying functional gene expression in microbial ecosystems. Trends Microbiol 14: 92–97 · DOI · Paper page
  142. Woyke T, Tighe D, Mavromatis K, Clum A, Copeland A, Schackwitz W, Lapidus A, Wu D, McCutcheon JP, McDonald BR, Moran NA, Bristow J, Cheng JF (2010) One bacterial cell, one complete genome. PLoS One 5: e10314 · DOI
  143. Woyke T, Xie G, Copeland A, Gonzalez JM, Han C, Kiss H, Saw JH, Senin P, Yang C, Chatterji S, Cheng JF, Eisen JA, Sieracki ME, Stepanauskas R (2009) Assembling the marine metagenome, one cell at a time. PLoS One 4: e5299 · DOI · Paper page
  144. Wu D, Hugenholtz P, Mavromatis K, Pukall R, Dalin E, Ivanova NN, Kunin V, Goodwin L, Wu M, Tindall BJ, Hooper SD, Pati A, Lykidis A, Spring S, Anderson IJ, D'Haeseleer P, Zemla A, Singer M, Lapidus A, Nolan M et al (2009) A phylogeny‐driven genomic encyclopaedia of Bacteria and Archaea. Nature 462: 1056–1060 · DOI · Paper page
  145. Wu M, Scott AJ (2012) Phylogenomic analysis of bacterial and archaeal sequences with AMPHORA2. Bioinformatics 28: 1033–1034 · DOI · Paper page
  146. Ye Y, Tang H (2009) An ORFome assembly approach to metagenomics sequences analysis. J Bioinform Comput Biol 7: 455–471 · DOI
  147. Zengler K, Palsson BO (2012) A road map for the development of community systems (CoSy) biology. Nat Rev Microbiol 10: 366–372 · DOI

Cited by

See all 326

Metadata

Authors
Segata, N., Boernigen, D., Tickle, T. L., Morgan, X. C., Garrett, W. S., & Huttenhower, C.
Venue
Molecular Systems Biology
Published
2013-01
Volume
9
Issue
1
Pages
666-666
ISSN
1744-4292 (ISSN-L)
OpenAlex
W2115057945
Cited by
326
References
28
FWCI
15.20
Type
journal article
Language
en
Open access
gold
Licence

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review

How to cite

Cite CoChat for the checks on this page, and the paper for its own findings.

This page
CoChat. (2026). Citation check: Computational meta'omics for microbial community studies. https://app.cochat.ai/papers/10.1038/msb.2013.22
The paper
Segata, N., Boernigen, D., Tickle, T. L., Morgan, X. C., Garrett, W. S., & Huttenhower, C. (2013). Computational meta'omics for microbial community studies. Molecular Systems Biology. https://doi.org/10.1038/msb.2013.22

Data sources

Bibliographic data: Semantic Scholar, OpenAlex, Crossref.

Contains information from the Semantic Scholar Academic Graph Datasets, made available under the ODC Attribution License (ODC-BY 1.0).

Semantic Scholar’s data is described in: Kinney, R., et al. (2023). The Semantic Scholar Open Data Platform. arXiv:2301.10140.