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High throughput sequencing methods for microbiome profiling: application to food animal systems

Published online by Cambridge University Press:  04 July 2012

Sarah K. Highlander*
Affiliation:
Department of Molecular Virology and Microbiology, Human Genome Sequencing Center, Baylor College of Medicine, Houston, TX 77030USA
*
*Corresponding author. E-mail: [email protected]

Abstract

Analysis of microbial communities using high throughput sequencing methods began in the mid 2000s permitting the production of 1000s to 10,000s of sequence reads per sample and megabases of data per sequence run. This then unprecedented depth of sequencing allowed, for the first time, the discovery of the ‘rare biosphere’ in environmental samples. The technology was quickly applied to studies in several human subjects. Perhaps these early studies served as a reminder that though the microbes that inhabit mammals are known to outnumber host cells by an order of magnitude or more, most of these are unknown members of our second genome, or microbiome (as coined by Joshua Lederberg), because of our inability to culture them. High throughput methods for microbial 16S ribosomal RNA gene and whole genome shotgun (WGS) sequencing have now begun to reveal the composition and identity of archaeal, bacterial and viral communities at many sites, in and on the human body. Surveys of the microbiota of food production animals have been published in the past few years and future studies should benefit from protocols and tools developed from large-scale human microbiome studies. Nevertheless, production animal-related resources, such as improved host genome assemblies and increased numbers and diversity of host-specific microbial reference genome sequences, will be needed to permit meaningful and robust analysis of 16S rDNA and WGS sequence data.

Type
Review Article
Copyright
Copyright © Cambridge University Press 2012

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References

Allander, T, Emerson, SU, Engle, RE, Purcell, RH and Bukh, J (2001). A virus discovery method incorporating DNase treatment and its application to the identification of two bovine parvovirus species. Proceedings of the National Academy of Sciences of the United States of America 98: 1160911614.CrossRefGoogle Scholar
Angiuoli, SV, Matalka, M, Gussman, A, Galens, K, Vangala, M, Riley, DR, Arze, C, White, JR, White, O and Fricke, WF (2011). CloVR: a virtual machine for automated and portable sequence analysis from the desktop using cloud computing. BMC Bioinformatics 12: 356.CrossRefGoogle ScholarPubMed
Bahl, MI, Bergstrom, A and Licht, TR (2012). Freezing fecal samples prior to DNA extraction affects the Firmicutes to Bacteroidetes ratio determined by downstream quantitative PCR analysis. FEMS Microbiology Letters 329: 193197.CrossRefGoogle ScholarPubMed
Bartram, AK, Lynch, MD, Stearns, JC, Moreno-Hagelsieb, G and Neufeld, JD (2011). Generation of multimillion-sequence 16S rRNA gene libraries from complex microbial communities by assembling paired-end illumina reads. Applied and Environmental Microbiology 77: 38463852.CrossRefGoogle ScholarPubMed
Bateman, A, Coin, L, Durbin, R, Finn, RD, Hollich, V, Griffiths-Jones, S, Khanna, A, Marshall, M, Moxon, S, Sonnhammer, EL, Studholme, DJ, Yeats, C and Eddy, SR (2004). The Pfam protein families database. Nucleic Acids Research 32: D138D141.CrossRefGoogle ScholarPubMed
Beja, O, Aravind, L, Koonin, EV, Suzuki, MT, Hadd, A, Nguyen, LP, Jovanovich, SB, Gates, CM, Feldman, RA, Spudich, JL, Spudich, EN and Delong, EF (2000a). Bacterial rhodopsin: evidence for a new type of phototrophy in the sea. Science 289: 19021906.CrossRefGoogle ScholarPubMed
Beja, O, Suzuki, MT, Koonin, EV, Aravind, L, Hadd, A, Nguyen, LP, Villacorta, R, Amjadi, M, Garrigues, C, Jovanovich, SB, Feldman, RA and Delong, EF (2000b). Construction and analysis of bacterial artificial chromosome libraries from a marine microbial assemblage. Environmental Microbiology 2: 516529.CrossRefGoogle ScholarPubMed
Bentley, DR, Balasubramanian, S, Swerdlow, HP, Smith, GP, Milton, J, Brown, CG, Hall, KP, Evers, DJ, Barnes, CL, Bignell, HR, Boutell, JM, Bryant, J, Carter, RJ, Keira Cheetham, R, Cox, AJ, Ellis, DJ, Flatbush, MR, Gormley, NA, Humphray, SJ, Irving, LJ, Karbelashvili, MS, Kirk, SM, Li, H, Liu, X, Maisinger, KS, Murray, LJ, Obradovic, B, Ost, T, Parkinson, ML, Pratt, MR, Rasolonjatovo, IM, Reed, MT, Rigatti, R, Rodighiero, C, Ross, MT, Sabot, A, Sankar, SV, Scally, A, Schroth, GP, Smith, ME, Smith, VP, Spiridou, A, Torrance, PE, Tzonev, SS, Vermaas, EH, Walter, K, Wu, X, Zhang, L, Alam, MD, Anastasi, C, Aniebo, IC, Bailey, DM, Bancarz, IR, Banerjee, S, Barbour, SG, Baybayan, PA, Benoit, VA, Benson, KF, Bevis, C, Black, PJ, Boodhun, A, Brennan, JS, Bridgham, JA, Brown, RC, Brown, AA, Buermann, DH, Bundu, AA, Burrows, JC, Carter, NP, Castillo, N, Chiara, ECM, Chang, S, Neil Cooley, R, Crake, NR, Dada, OO, Diakoumakos, KD, Dominguez-Fernandez, B, Earnshaw, DJ, Egbujor, UC, Elmore, DW, Etchin, SS, Ewan, MR, Fedurco, M, Fraser, LJ, Fuentes Fajardo, KV, Scott Furey, W, George, D, Gietzen, KJ, Goddard, CP, Golda, GS, Granieri, PA, Green, DE, Gustafson, DL, Hansen, NF, Harnish, K, Haudenschild, CD, Heyer, NI, Hims, MM, Ho, JT, Horgan, AM, Hoschler, K, Hurwitz, S, Ivanov, DV, Johnson, MQ, James, T, Huw Jones, TA, Kang, GD, Kerelska, TH, Kersey, AD, Khrebtukova, I, Kindwall, AP, Kingsbury, Z, Kokko-Gonzales, PI, Kumar, A, Laurent, MA, Lawley, CT, Lee, SE, Lee, X, Liao, AK, Loch, JA, Lok, M, Luo, S, Mammen, RM, Martin, JW, McCauley, PG, McNitt, P, Mehta, P, Moon, KW, Mullens, JW, Newington, T, Ning, Z, Ling Ng, B, Novo, SM, O'Neill, MJ, Osborne, MA, Osnowski, A, Ostadan, O, Paraschos, LL, Pickering, L, Pike, AC, Pike, AC, Chris Pinkard, D, Pliskin, DP, Podhasky, J, Quijano, VJ, Raczy, C, Rae, VH, Rawlings, SR, Chiva Rodriguez, A, Roe, PM, Rogers, J, Rogert Bacigalupo, MC, Romanov, N, Romieu, A, Roth, RK, Rourke, NJ, Ruediger, ST, Rusman, E, Sanches-Kuiper, RM, Schenker, MR, Seoane, JM, Shaw, RJ, Shiver, MK, Short, SW, Sizto, NL, Sluis, JP, Smith, MA, Ernest Sohna Sohna, J, Spence, EJ, Stevens, K, Sutton, N, Szajkowski, L, Tregidgo, CL, Turcatti, G, Vandevondele, S, Verhovsky, Y, Virk, SM, Wakelin, S, Walcott, GC, Wang, J, Worsley, GJ, Yan, J, Yau, L, Zuerlein, M, Rogers, J, Mullikin, JC, Hurles, ME, McCooke, NJ, West, JS, Oaks, FL, Lundberg, PL, Klenerman, D, Durbin, R and Smith, AJ (2008). Accurate whole human genome sequencing using reversible terminator chemistry. Nature 456: 5359.CrossRefGoogle ScholarPubMed
Berg Miller, ME, Yeoman, CJ, Chia, N, Tringe, SG, Angly, FE, Edwards, RA, Flint, HJ, Lamed, R, Bayer, EA and White, BA (2012). Phage-bacteria relationships and CRISPR elements revealed by a metagenomic survey of the rumen microbiome. Environmental Microbiology 14: 207227.CrossRefGoogle ScholarPubMed
Binga, EK, Lasken, RS and Neufeld, JD (2008). Something from (almost) nothing: the impact of multiple displacement amplification on microbial ecology. ISME Journal 2: 233241.CrossRefGoogle ScholarPubMed
Bretschger, O, Osterstock, JB, Pinchak, WE, Ishii, S and Nelson, KE (2010). Microbial fuel cells and microbial ecology: applications in ruminant health and production research. Microbial Ecology 59: 415427.CrossRefGoogle ScholarPubMed
Brulc, JM, Antonopoulos, DA, Miller, ME, Wilson, MK, Yannarell, AC, Dinsdale, EA, Edwards, RE, Frank, ED, Emerson, JB, Wacklin, P, Coutinho, PM, Henrissat, B, Nelson, KE and White, BA (2009). Gene-centric metagenomics of the fiber-adherent bovine rumen microbiome reveals forage specific glycoside hydrolases. Proceedings of the National Academy of Sciences of the United States of America 106: 19481953.CrossRefGoogle ScholarPubMed
Caporaso, JG, Lauber, CL, Walters, WA, Berg-Lyons, D, Lozupone, CA, Turnbaugh, PJ, Fierer, N and Knight, R (2011). Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample. Proceedings of the National Academy of Sciences of the United States of America 108 (suppl. 1): 45164522.CrossRefGoogle Scholar
Chao, A (1984). Non-parametric estimation of the number of classes in a population. Scandinavian Journal of Statistics 11: 265270.Google Scholar
Claudel-Renard, C, Chevalet, C, Faraut, T and Kahn, D (2003). Enzyme-specific profiles for genome annotation: PRIAM. Nucleic Acids Research 31: 66336639.CrossRefGoogle ScholarPubMed
Cole, JR, Wang, Q, Cardenas, E, Fish, J, Chai, B, Farris, RJ, Kulam-Syed-Mohideen, AS, McGarrell, DM, Marsh, T, Garrity, GM and Tiedje, JM (2009). The Ribosomal Database Project: improved alignments and new tools for rRNA analysis. Nucleic Acids Research 37: D141D145.CrossRefGoogle ScholarPubMed
Danzeisen, JL, Kim, HB, Isaacson, RE, Tu, ZJ and Johnson, TJ (2011). Modulations of the chicken cecal microbiome and metagenome in response to anticoccidial and growth promoter treatment. Public Library of Science ONE 6: e27949.Google ScholarPubMed
Day, JM, Ballard, LL, Duke, MV, Scheffler, BE and Zsak, L (2010). Metagenomic analysis of the turkey gut RNA virus community. Virology Journal 7: 313.CrossRefGoogle ScholarPubMed
Dowd, SE, Callaway, TR, Wolcott, RD, Sun, Y, McKeehan, T, Hagevoort, RG and Edrington, TS (2008). Evaluation of the bacterial diversity in the feces of cattle using 16S rDNA bacterial tag-encoded FLX amplicon pyrosequencing (bTEFAP). BMC Microbiology 8: 125.CrossRefGoogle ScholarPubMed
Durso, LM, Harhay, GP, Bono, JL and Smith, TP (2011a). Virulence-associated and antibiotic resistance genes of microbial populations in cattle feces analyzed using a metagenomic approach. Journal of Microbiological Methods 84: 278282.CrossRefGoogle ScholarPubMed
Durso, LM, Harhay, GP, Smith, TP, Bono, JL, Desantis, TZ and Clawson, ML (2011b). Bacterial community analysis of beef cattle feedlots reveals that pen surface is distinct from feces. Foodborne Pathogens and Disease 8: 647649.CrossRefGoogle ScholarPubMed
Edgar, RC, Haas, BJ, Clemente, JC, Quince, C and Knight, R (2011). UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27: 21942200.CrossRefGoogle ScholarPubMed
Edwards, RA and Rohwer, F (2005). Viral metagenomics. Nature Reviews Microbiology 3: 504510.CrossRefGoogle ScholarPubMed
Edwards, RA, Rodriguez-Brito, B, Wegley, L, Haynes, M, Breitbart, M, Peterson, DM, Saar, MO, Alexander, S, Alexander, EC Jr and Rohwer, F (2006). Using pyrosequencing to shed light on deep mine microbial ecology. BMC Genomics 7: 57.CrossRefGoogle ScholarPubMed
Federhen, S (2012). The NCBI Taxonomy database. Nucleic Acids Research 40: D136–143.CrossRefGoogle ScholarPubMed
Frank, JA, Reich, CI, Sharma, S, Weisbaum, JS, Wilson, BA and Olsen, GJ (2008). Critical evaluation of two primers commonly used for amplification of bacterial 16S rRNA genes. Applied and Environmental Microbiology 74: 24612470.CrossRefGoogle ScholarPubMed
Gerlach, W, Junemann, S, Tille, F, Goesmann, A and Stoye, J (2009). WebCARMA: a web application for the functional and taxonomic classification of unassembled metagenomic reads. BMC Bioinformatics 10: 430.CrossRefGoogle ScholarPubMed
Glad, T, Bernhardsen, P, Nielsen, KM, Brusetti, L, Andersen, M, Aars, J and Sundset, MA (2010). Bacterial diversity in faeces from polar bear (Ursus maritimus) in Arctic Svalbard. BMC Microbiology 10: 10.CrossRefGoogle ScholarPubMed
Goll, J, Rusch, DB, Tanenbaum, DM, Thiagarajan, M, Li, K, Methe, BA and Yooseph, S (2010). METAREP: JCVI metagenomics reports – an open source tool for high-performance comparative metagenomics. Bioinformatics 26: 26312632.CrossRefGoogle ScholarPubMed
Gutell, RR, Larsen, N and Woese, CR (1994). Lessons from an evolving rRNA: 16S and 23S rRNA structures from a comparative perspective. Microbiological Reviews 58: 1026.CrossRefGoogle ScholarPubMed
Haft, DH, Selengut, JD and White, O (2003). The TIGRFAMs database of protein families. Nucleic Acids Research 31: 371373.CrossRefGoogle ScholarPubMed
Hess, M, Sczyrba, A, Egan, R, Kim, TW, Chokhawala, H, Schroth, G, Luo, S, Clark, DS, Chen, F, Zhang, T, Mackie, RI, Pennacchio, LA, Tringe, SG, Visel, A, Woyke, T, Wang, Z and Rubin, EM (2011). Metagenomic discovery of biomass-degrading genes and genomes from cow rumen. Science 331: 463467.CrossRefGoogle ScholarPubMed
Hoffmann, B, Scheuch, M, Hoper, D, Jungblut, R, Holsteg, M, Schirrmeier, H, Eschbaumer, M, Goller, KV, Wernike, K, Fischer, M, Breithaupt, A, Mettenleiter, TC and Beer, M (2012). Novel orthobunyavirus in cattle, Europe, 2011. Emerging Infectious Diseases 18: 469472.CrossRefGoogle ScholarPubMed
Horvath, P and Barrangou, R (2010). CRISPR/Cas, the immune system of bacteria and archaea. Science 327: 167170.CrossRefGoogle ScholarPubMed
Huse, SM, Huber, JA, Morrison, HG, Sogin, ML and Welch, DM (2007). Accuracy and quality of massively parallel DNA pyrosequencing. Genome Biology 8: R143.CrossRefGoogle ScholarPubMed
Huttenhower, C, Gevers, D, Knight, R, Abubucker, S, Badger, J, Chinwalla, A, Creasy, H, Earl, A, Fitzgerald, M, Fulton, R, Giglio, M, Pepin, K, Lobos, E, Madupu, R, Magrini, V, Martin, J, Mitreva, M, Muzny, D, Sodergren, E, Versalovic, J, Wollam, A, Worley, K, Wortman, J, Young, S, Zeng, Q, Aagaard, K, Allen-Vercoe, E, Alm, E, Alvarado, L, Andersen, G, Anderson, S, Appelbaum, E, Arachchi, H, Armitage, G, Arze, C, Ayvaz, T, Baker, C, Begg, L, Belachew, T, Bihan, M, Blaser, M, Bloom, T, Bonazzi, V, Brooks, J, Buck, G, Buhay, C, Busam, D, Campbell, J, Canon, R, Cantarel, B, Chen, I-M, Chhibba, S, Chu, K, Ciulla, D, Clemente, J, Clifton, S, Conlan, S, Crabtree, J, Cutting, M, Davidovics, N, Davis, C, Desantis, T, Deal, C, Delehaunty, K, Dewhirst, F, Deych, E, Dooling, D, Dugan, S, Dunne, W, Durkin, A, Edgar, R, Erlich, R, Farmer, C, Farrell, R, Faust, K, Feldgarden, M, Felix, V, Fisher, S, Fodor, A, Forney, L, Foster, L, Di Francesco, V, Friedman, J, Friedrich, D, Fronick, C, Fulton, L, Gao, H, Garcia, N, Giannoukos, G, Giblin, C, Giovanni, M, Goldberg, J, Goll, J, Gonzalez, A, Gujja, S, Haake, S, Haas, B, Hamilton, H, Harris, E, Hepburn, T, Herter, B, Hoffmann, D, Holder, M, Huang, K, Huse, S, Izard, J, Jansson, J, Jiang, H, Jordan, C, Joshi, V, Katancik, J, Keitel, W, Kelley, S, Kells, C, King, N, Knights, D, Kong, H, Koren, O, Kota, K, Kovar, C, Kyrpides, N, Lee, S, Lemon, K, Lennon, N, Lewis, C, Lewis, L, Ley, R, Li, K, Liolios, K, Liu, Y, Lozupone, C, Lunsford, R, Madden, T, Mahurkar, A, Mannon, P, Mardis, E, Markowitz, V, McDonald, D, McEwen, J, McGuire, A, McInnes, P, Mehta, T, Mihindukulasuriya, K, Newsham, I, Nusbaum, C, O'laughlin, M, Orvis, J, Pagani, I, Palaniappan, K, Patel, S, Pearson, M, Peterson, J, Podar, M, Pohl, C, Pollard, K, Pop, M, Priest, M, Proctor, L, Qin, X, Raes, J, Reid, J, Rhodes, R, Riehle, K, Rivera, M, Rodriguez-Mueller, B, Rogers, Y-H, La Rosa, P, Ross, M, Russ, C, Sanka, R, Sankar, P, Sathirapongsasuti, J, Schloss, J, Schloss, P, Schmidt, T, Schriml, L, Schubert, A, Segata, N, Segre, J, Shannon, W, Sharp, R, Sharpton, T, Shenoy, N, Sheth, N, Simone, G, Singh, I, Smillie, C, Sobel, J, Spicer, P, Sutton, G, Sykes, S, Tabbaa, D, Thiagarajan, M, Tomlinson, C, Torralba, M, Truty, R, Vishnivetskaya, T, Walker, J, Wang, L, Wang, Z, Ward, D, Watson, M, Wellington, C, Wetterstrand, K, White, J, Wilczek-Boney, K, Wu, Y, Wylie, K, Wylie, T, Yandava, C, Ye, Y, Yooseph, S, Youmans, B, Zhang, L, Zhou, Y, Zhu, Y, Zoloth, L, Zucker, J, Birren, B, Gibbs, R, Highlander, S, Methé, B, Nelson, K, Petrosino, J, Weinstock, G, Wilson, R, White, O, Griggs, A, Liu, B, Lo, C-C, Howarth, C, Sommer, D, McCorrison, J, Miller, J, Mavromatis, K, Chen, L, Ye, L, Scholz, M, Rho, M, Abolude, O, Minx, P, Chain, P, Koren, S, Treangen, T, Bhonagiri, V, Warren, W, Ding, Y and Ravel, J (2012). Structure, function and diversity of the healthy human microbiome. Nature 486: 875922.Google Scholar
Jami, E and Mizrahi, I (2012). Composition and similarity of bovine rumen microbiota across individual animals. Public Library of Science ONE 7: e33306.Google ScholarPubMed
Kanehisa, M and Goto, S (2000). KEGG: Kyoto encyclopedia of genes and genomes. Nucleic Acids Research 28: 2730.CrossRefGoogle ScholarPubMed
Kav, AB, Sasson, G, Jami, E, Doron-Faigenboim, A, Benhar, I and Mizrahi, I (2012). Insights into the bovine rumen plasmidome. Proceedings of the National Academy of Sciences of the United States of America 109: 54525457.CrossRefGoogle Scholar
Kuczynski, J, Stombaugh, J, Walters, WA, Gonzalez, A, Caporaso, JG and Knight, R (2011). Using QIIME to analyze 16S rRNA gene sequences from microbial communities. Current Protocols in Bioinformatics Chapter 10: Unit 10 17. 934935.Google ScholarPubMed
Lamendella, R, Domingo, JW, Ghosh, S, Martinson, J and Oerther, DB (2011). Comparative fecal metagenomics unveils unique functional capacity of the swine gut. BMC Microbiology 11: 103.CrossRefGoogle ScholarPubMed
Lan, Y, Wang, Q, Cole, JR and Rosen, GL (2012). Using the RDP classifier to predict taxonomic novelty and reduce the search space for finding novel organisms. Public Library of Science ONE 7: e32491.Google ScholarPubMed
Lane, DJ (1991). 16S/23S rRNA sequencing. In: Stackebrandt, E and Goodfellow, M (eds) Nucleic acid Techniques in Bacterial Systematics, Chichester, England: John Wiley & Sons, pp. 115175.Google Scholar
Lauber, CL, Zhou, N, Gordon, JI, Knight, R and Fierer, N (2010). Effect of storage conditions on the assessment of bacterial community structure in soil and human-associated samples. FEMS Microbiology Letters 307: 8086.CrossRefGoogle ScholarPubMed
Lazarevic, V, Whiteson, K, Huse, S, Hernandez, D, Farinelli, L, Osteras, M, Schrenzel, J and Francois, P (2009). Metagenomic study of the oral microbiota by Illumina high-throughput sequencing. Journal of Microbiological Methods 79: 266271.CrossRefGoogle ScholarPubMed
Ley, RE, Hamady, M, Lozupone, C, Turnbaugh, PJ, Ramey, RR, Bircher, JS, Schlegel, ML, Tucker, TA, Schrenzel, MD, Knight, R and Gordon, JI (2008). Evolution of mammals and their gut microbes. Science 320: 16471651.CrossRefGoogle ScholarPubMed
Li, H and Durbin, R (2009). Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25: 17541760.CrossRefGoogle ScholarPubMed
Li, R, Zhu, H, Ruan, J, Qian, W, Fang, X, Shi, Z, Li, Y, Li, S, Shan, G, Kristiansen, K, Li, S, Yang, H, Wang, J and Wang, J (2010). De novo assembly of human genomes with massively parallel short read sequencing. Genome Research 20: 265272.CrossRefGoogle ScholarPubMed
Li, RW, Connor, EE, Li, C, Baldwin Vi, RL and Sparks, ME (2012). Characterization of the rumen microbiota of pre-ruminant calves using metagenomic tools. Environmental Microbiology 14: 129139.CrossRefGoogle ScholarPubMed
Li, RW, Wu, S, Li, W, Huang, Y and Gasbarre, LC (2011). Metagenome plasticity of the bovine abomasal microbiota in immune animals in response to Ostertagia ostertagi infection. Public Library of Science ONE 6: e24417.Google ScholarPubMed
Liu, B, Gibbons, T, Ghodsi, M, Treangen, T and Pop, M (2011). Accurate and fast estimation of taxonomic profiles from metagenomic shotgun sequences. BMC Genomics 12 (suppl. 2): S4.CrossRefGoogle ScholarPubMed
Lowe, BA, Marsh, TL, Isaacs-Cosgrove, N, Kirkwood, RN, Kiupel, M and Mulks, MH (2011). Microbial communities in the tonsils of healthy pigs. Veterinary Microbiology 147: 346357.CrossRefGoogle ScholarPubMed
Lowe, BA, Marsh, TL, Isaacs-Cosgrove, N, Kirkwood, RN, Kiupel, M and Mulks, MH (2012). Defining the “core microbiome” of the microbial communities in the tonsils of healthy pigs. BMC Microbiology 12: 20.CrossRefGoogle ScholarPubMed
Lozupone, C and Knight, R (2005). UniFrac: a new phylogenetic method for comparing microbial communities. Applied and Environmental Microbiology 71: 82288235.CrossRefGoogle ScholarPubMed
Lozupone, C, Lladser, ME, Knights, D, Stombaugh, J and Knight, R (2011). UniFrac: an effective distance metric for microbial community comparison. ISME Journal 5: 169172.CrossRefGoogle ScholarPubMed
Lozupone, CA and Knight, R (2008). Species divergence and the measurement of microbial diversity. FEMS Microbiology Reviews 32: 557578.CrossRefGoogle ScholarPubMed
Magurran, AE (1988). Ecological Diversity and its Measurement. Princeton, NJ: Princeton University Press.CrossRefGoogle Scholar
Margulies, M, Egholm, M, Altman, WE, Attiya, S, Bader, JS, Bemben, LA, Berka, J, Braverman, MS, Chen, YJ, Chen, Z, Dewell, SB, Du, L, Fierro, JM, Gomes, XV, Godwin, BC, He, W, Helgesen, S, Ho, CH, Irzyk, GP, Jando, SC, Alenquer, ML, Jarvie, TP, Jirage, KB, Kim, JB, Knight, JR, Lanza, JR, Leamon, JH, Lefkowitz, SM, Lei, M, Li, J, Lohman, KL, Lu, H, Makhijani, VB, McDade, KE, McKenna, MP, Myers, EW, Nickerson, E, Nobile, JR, Plant, R, Puc, BP, Ronan, MT, Roth, GT, Sarkis, GJ, Simons, JF, Simpson, JW, Srinivasan, M, Tartaro, KR, Tomasz, A, Vogt, KA, Volkmer, GA, Wang, SH, Wang, Y, Weiner, MP, Yu, P, Begley, RF and Rothberg, JM (2005). Genome sequencing in microfabricated high-density picolitre reactors. Nature 437: 376380.CrossRefGoogle ScholarPubMed
Markowitz, VM, Chen, IM, Chu, K, Szeto, E, Palaniappan, K, Grechkin, Y, Ratner, A, Jacob, B, Pati, A, Huntemann, M, Liolios, K, Pagani, I, Anderson, I, Mavromatis, K, Ivanova, NN and Kyrpides, NC (2012). IMG/M: the integrated metagenome data management and comparative analysis system. Nucleic Acids Research 40: D123–129.CrossRefGoogle ScholarPubMed
Markowitz, VM, Chen, IM, Palaniappan, K, Chu, K, Szeto, E, Grechkin, Y, Ratner, A, Anderson, I, Lykidis, A, Mavromatis, K, Ivanova, NN and Kyrpides, NC (2010). The integrated microbial genomes system: an expanding comparative analysis resource. Nucleic Acids Research 38: D382–390.CrossRefGoogle ScholarPubMed
Matsuki, T, Watanabe, K, Fujimoto, J, Miyamoto, Y, Takada, T, Matsumoto, K, Oyaizu, H and Tanaka, R (2002). Development of 16S rRNA-gene-targeted group-specific primers for the detection and identification of predominant bacteria in human feces. Applied and Environmental Microbiology 68: 54455451.CrossRefGoogle ScholarPubMed
McDonald, D, Price, MN, Goodrich, J, Nawrocki, EP, Desantis, TZ, Probst, A, Andersen, GL, Knight, R and Hugenholtz, P (2012). An improved Greengenes taxonomy with explicit ranks for ecological and evolutionary analyses of bacteria and archaea. ISME Journal 6: 610618.CrossRefGoogle ScholarPubMed
Methé, B, Nelson, KE, Pop, M, Creasy, HH, Giglio, MG, Huttenhower, C, Gevers, D, Petrosino, JF, Abubucker, S, Badger, JH, Chinwalla, AT, Earl, AM, Fitzgerald, MG, Fulton, RS, Hallsworth-Pepin, K, Lobos, EA, Madupu, R, Magrini, V, Martin, JC, Mitreva, M, Muzny, DM, Sodergren, EJ, Versalovic, J, Wollam, AM, Worley, KC, Wortman, JR, Young, SK, Zeng, Q, Aagaard, KM, Allen-Vercoe, E, Alm, EJ, Alvarado, L, Andersen, GL, Anderson, S, Appelbaum, E, Arachchi, HM, Armitage, G, Arze, CA, Ayvaz, T, Baker, CC, Begg, L, Belachew, T, Bihan, M, Blaser, M, Bloom, T, Bonazzi, V, Brooks, JP, Buck, GA, Buhay, CJ, Busam, DA, Campbell, JL, Canon, SR, Cantarel, BL, Chen, I-MA, Chhibba, S, Chu, K, Ciulla, DM, Clemente, JC, Clifton, SW, Conlan, S, Crabtree, J, Cutting, MA, Davidovics, NJ, Davis, CC, Desantis, TZ, Deal, C, Delehaunty, KD, Dewhirst, FE, Deych, E, Dooling, DJ, Dugan, SP, Dunne, WM, Durkin, AS, Edgar, RC, Erlich, RL, Farmer, CN, Farrell, RM, Faust, K, Feldgarden, M, Felix, VM, Fisher, S, Fodor, AA, Forney, L, Foster, L, Di Francesco, V, Friedman, J, Friedrich, DC, Fronick, CC, Fulton, LL, Gao, H, Garcia, N, Giannoukos, G, Giblin, C, Giovanni, MY, Goldberg, JM, Goll, J, Gonzalez, A, Gujja, S, Haake, SKHaas, BJ, Hamilton, HA, Harris, EL, Hepburn, TA, Herter, B, Hoffmann, DE, Holder, ME, Huang, KH, Huse, SM, Izard, J, Jansson, JK, Jiang, H, Jordan, C, Joshi, V, Katancik, JA, Keitel, WA, Kelley, ST, Kells, C, King, NB, Knight, R, Knights, D, Kong, HH, Koren, O, Kota, KC, Kovar, CL, Kyrpides, NC, Lee, SL, Lemon, KP, Lennon, N, Lewis, CM, Lewis, L, Ley, RE, Li, K, Liolios, K, Liu, Y, Lozupone, CA, Lunsford, RD, Madden, T, Mahurkar, AA, Mannon, PJ, Mardis, ER, Markowitz, VM, McDonald, D, McEwen, J, McGuire, AL, McInnes, P, Mehta, T, Mihindukulasuriya, KA, Newsham, I, Nusbaum, C, O'Laughlin, M, Orvis, J, Pagani, I, Palaniappan, K, Patel, SM, Pearson, M, Peterson, J, Podar, M, Pohl, C, Pollard, KS, Priest, ME, Proctor, LM, Qin, X, Raes, J, Reid, JG, Rhodes, R, Riehle, KP, Rivera, MC, Rodriguez-Mueller, B, Rogers, Y-H, La Rosa, PS, Ross, MC, Russ, C, Sanka, RK, Sankar, P, Sathirapongsasuti, JF, Schloss, JA, Schloss, PD, Schmidt, TM, Schriml, L, Schubert, AM, Segata, N, Segre, JA, Shannon, WD, Sharp, RR, Sharpton, TJ, Shenoy, N, Sheth, NU, Simone, GA, Singh, I, Smillie, CS, Sobel, JD, Spicer, P, Sutton, GG, Sykes, SM, Tabbaa, DG, Thiagarajan, M, Tomlinson, CM, Torralba, M, Truty, RM, Vishnivetskaya, TA, Walker, J, Wang, L, Wang, Z, Ward, DV, Watson, MA, Wellington, C, Wetterstrand, KA, White, JR, Wilczek-Boney, K, Wu, YQ, Wylie, KM, Wylie, T, Yandava, C, Ye, Y, Yooseph, S, Youmans, BP, Zhang, L, Zhou, Y, Zhu, Y, Zoloth, L, Zucker, JD, Birren, BW, Gibbs, RA, Highlander, SK, Weinstock, GM, and Wilson, RK (2012). A framework for human microbiome research. Nature 486: 10341080.Google Scholar
Meyer, F, Paarmann, D, D'souza, M, Olson, R, Glass, EM, Kubal, M, Paczian, T, Rodriguez, A, Stevens, R, Wilke, A, Wilkening, J and Edwards, RA (2008). The metagenomics RAST server – a public resource for the automatic phylogenetic and functional analysis of metagenomes. BMC Bioinformatics 9: 386.CrossRefGoogle Scholar
Mitra, S, Stark, M and Huson, DH (2011). Analysis of 16S rRNA environmental sequences using MEGAN. BMC Genomics 12 (suppl. 3): S17.CrossRefGoogle ScholarPubMed
Nelson, KE, Weinstock, GM, Highlander, SK, Worley, KC, Creasy, HH, Wortman, JR, Rusch, DB, Mitreva, M, Sodergren, E, Chinwalla, AT, Feldgarden, M, Gevers, D, Haas, BJ, Madupu, R, Ward, DV, Birren, BW, Gibbs, RA, Methe, B, Petrosino, JF, Strausberg, RL, Sutton, GG, White, OR, Wilson, RK, Durkin, S, Giglio, MG, Gujja, S, Howarth, C, Kodira, CD, Kyrpides, N, Mehta, T, Muzny, DM, Pearson, M, Pepin, K, Pati, A, Qin, X, Yandava, C, Zeng, Q, Zhang, L, Berlin, AM, Chen, L, Hepburn, TA, Johnson, J, McCorrison, J, Miller, J, Minx, P, Nusbaum, C, Russ, C, Sykes, SM, Tomlinson, CM, Young, S, Warren, WC, Badger, J, Crabtree, J, Markowitz, VM, Orvis, J, Cree, A, Ferriera, S, Fulton, LL, Fulton, RS, Gillis, M, Hemphill, LD, Joshi, V, Kovar, C, Torralba, M, Wetterstrand, KA, Abouellleil, A, Wollam, AM, Buhay, CJ, Ding, Y, Dugan, S, FitzGerald, MG, Holder, M, Hostetler, J, Clifton, SW, Allen-Vercoe, E, Earl, AM, Farmer, CN, Liolios, K, Surette, MG, Xu, Q, Pohl, C, Wilczek-Boney, K and Zhu, D (2010). A catalog of reference genomes from the human microbiome. Science 328: 994999.Google ScholarPubMed
Noguchi, H, Taniguchi, T and Itoh, T (2008). MetaGeneAnnotator: detecting species-specific patterns of ribosomal binding site for precise gene prediction in anonymous prokaryotic and phage genomes. DNA Research 15: 387396.CrossRefGoogle ScholarPubMed
Overbeek, R, Begley, T, Butler, RM, Choudhuri, JV, Chuang, HY, Cohoon, M, De Crecy-Lagard, V, Diaz, N, Disz, T, Edwards, R, Fonstein, M, Frank, ED, Gerdes, S, Glass, EM, Goesmann, A, Hanson, A, Iwata-Reuyl, D, Jensen, R, Jamshidi, N, Krause, L, Kubal, M, Larsen, N, Linke, B, McHardy, AC, Meyer, F, Neuweger, H, Olsen, G, Olson, R, Osterman, A, Portnoy, V, Pusch, GD, Rodionov, DA, Ruckert, C, Steiner, J, Stevens, R, Thiele, I, Vassieva, O, Ye, Y, Zagnitko, O and Vonstein, V (2005). The subsystems approach to genome annotation and its use in the project to annotate 1000 genomes. Nucleic Acids Research 33: 56915702.CrossRefGoogle Scholar
Ozutsumi, Y, Hayashi, H, Sakamoto, M, Itabashi, H and Benno, Y (2005). Culture-independent analysis of fecal microbiota in cattle. Bioscience Biotechnology and Biochemistry 69: 17931797.CrossRefGoogle ScholarPubMed
Poroyko, V, White, JR, Wang, M, Donovan, S, Alverdy, J, Liu, DC and Morowitz, MJ (2010). Gut microbial gene expression in mother-fed and formula-fed piglets. Public Library of Science ONE 5: e12459.Google ScholarPubMed
Pruesse, E, Quast, C, Knittel, K, Fuchs, BM, Ludwig, W, Peplies, J and Glockner, FO (2007). SILVA: a comprehensive online resource for quality checked and aligned ribosomal RNA sequence data compatible with ARB. Nucleic Acids Research 35: 71887196.CrossRefGoogle Scholar
Qu, A, Brulc, JM, Wilson, MK, Law, BF, Theoret, JR, Joens, LA, Konkel, ME, Angly, F, Dinsdale, EA, Edwards, RA, Nelson, KE and White, BA (2008). Comparative metagenomics reveals host specific metavirulomes and horizontal gene transfer elements in the chicken cecum microbiome. Public Library of Science ONE 3: e2945.Google ScholarPubMed
Reuter, G, Nemes, C, Boros, A, Kapusinszky, B, Delwart, E and Pankovics, P (2012). Astrovirus in wild boars (Sus scrofa) in Hungary. Archives of Virology 157: 11431147 [Epub ahead of print].CrossRefGoogle ScholarPubMed
Riboulet-Bisson, E, Sturme, MH, Jeffery, IB, O'donnell, MM, Neville, BA, Forde, BM, Claesson, MJ, Harris, H, Gardiner, GE, Casey, PG, Lawlor, PG, O'Toole, PW and Ross, RP (2012). Effect of Lactobacillus salivarius bacteriocin Abp118 on the mouse and pig intestinal microbiota. Public Library of Science ONE 7: e31113.Google ScholarPubMed
Samsudin, AA, Evans, PN, Wright, AD and Al Jassim, R (2011). Molecular diversity of the foregut bacteria community in the dromedary camel (Camelus dromedarius). Environmental Microbiology 13: 30243035.CrossRefGoogle ScholarPubMed
Sanger, F, Nicklen, S and Coulson, AR (1977). DNA sequencing with chain-terminating inhibitors. Proceedings of the National Academy of Sciences of the United States of America 74: 54635467.CrossRefGoogle ScholarPubMed
Schloss, PD (2008). Evaluating different approaches that test whether microbial communities have the same structure. ISME Journal 2: 265275.CrossRefGoogle ScholarPubMed
Schloss, PD, Westcott, SL, Ryabin, T, Hall, JR, Hartmann, M, Hollister, EB, Lesniewski, RA, Oakley, BB, Parks, DH, Robinson, CJ, Sahl, JW, Stres, B, Thallinger, GG, Van Horn, DJ and Weber, CF (2009). Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Applied and Environmental Microbiology 75: 75377541.CrossRefGoogle ScholarPubMed
Scupham, AJ, Patton, TG, Bent, E and Bayles, DO (2008). Comparison of the cecal microbiota of domestic and wild turkeys. Microbial Ecology 56: 322331.CrossRefGoogle ScholarPubMed
Shan, T, Li, L, Simmonds, P, Wang, C, Moeser, A and Delwart, E (2011). The fecal virome of pigs on a high-density farm. Journal of Virology 85: 1169711708.CrossRefGoogle ScholarPubMed
Shanks, OC, Kelty, CA, Archibeque, S, Jenkins, M, Newton, RJ, McLellan, SL, Huse, SM and Sogin, ML (2011). Community structures of fecal bacteria in cattle from different animal feeding operations. Applied and Environmental Microbiology 77: 29923001.CrossRefGoogle ScholarPubMed
Sim, K, Cox, MJ, Wopereis, H, Martin, R, Knol, J, Li, MS, Cookson, WO, Moffatt, MF and Kroll, JS (2012). Improved detection of Bifidobacteria with optimised 16S rRNA-gene based pyrosequencing. Public Library of Science ONE 7: e32543.Google ScholarPubMed
Sogin, ML, Morrison, HG, Huber, JA, Mark Welch, D, Huse, SM, Neal, PR, Arrieta, JM and Herndl, GJ (2006). Microbial diversity in the deep sea and the underexplored “rare biosphere”. Proceedings of the National Academy of Sciences of the United States of America 103: 1211512120.CrossRefGoogle ScholarPubMed
Sonnhammer, EL, Von Heijne, G and Krogh, A (1998). A hidden Markov model for predicting transmembrane helices in protein sequences. Proceedings of the International Conference on Intelligent Systems for Molecular Biology 6: 175182.Google ScholarPubMed
Suchodolski, JS, Camacho, J and Steiner, JM (2008). Analysis of bacterial diversity in the canine duodenum, jejunum, ileum, and colon by comparative 16S rRNA gene analysis. FEMS Microbiology Ecology 66: 567578.CrossRefGoogle ScholarPubMed
Sundset, MA, Edwards, JE, Cheng, YF, Senosiain, RS, Fraile, MN, Northwood, KS, Praesteng, KE, Glad, T, Mathiesen, SD and Wright, AD (2009). Rumen microbial diversity in Svalbard reindeer, with particular emphasis on methanogenic archaea. FEMS Microbiology Ecology 70: 553562.CrossRefGoogle ScholarPubMed
Tanenbaum, DM, Goll, J, Murphy, S, Kumar, P, Zafar, N, Thiagarajan, M, Madupu, R, Davidsen, T, Kagan, L, Kravitz, S, Rusch, DB and Yooseph, S (2010). The JCVI standard operating procedure for annotating prokaryotic metagenomic shotgun sequencing data. Standards in Genomic Sciences 2: 229237.CrossRefGoogle ScholarPubMed
Tringe, SG and Rubin, EM (2005). Metagenomics: DNA sequencing of environmental samples. Nature Reviews Genetics 6: 805814.CrossRefGoogle ScholarPubMed
Turnbaugh, PJ and Gordon, JI (2008). An invitation to the marriage of metagenomics and metabolomics. Cell 134: 708713.CrossRefGoogle Scholar
Venter, JC, Remington, K, Heidelberg, JF, Halpern, AL, Rusch, D, Eisen, JA, Wu, D, Paulsen, I, Nelson, KE, Nelson, W, Fouts, DE, Levy, S, Knap, AH, Lomas, MW, Nealson, K, White, O, Peterson, J, Hoffman, J, Parsons, R, Baden-Tillson, H, Pfannkoch, C, Rogers, YH and Smith, HO (2004). Environmental genome shotgun sequencing of the Sargasso Sea. Science 304: 6674.CrossRefGoogle ScholarPubMed
Wang, Q, Garrity, GM, Tiedje, JM and Cole, JR (2007). Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Applied and Environmental Microbiology 73: 52615267.CrossRefGoogle ScholarPubMed
Ward, DV and Jumpstart Consortium Human Microbiome Project Data Generation Working Group (2012). Evaluation of 16S rDNA-based community profiling for human microbiome research. Public Library of Science ONE: 12291232.Google Scholar
Woese, CR, Winker, S and Gutell, RR (1990). Architecture of ribosomal RNA: constraints on the sequence of ‘tetra-loops’. Proceedings of the National Academy of Sciences of the United States of America 87: 84678471.CrossRefGoogle ScholarPubMed
Wooley, JC, Godzik, A and Friedberg, I (2010). A primer on metagenomics. Public Library of Science Computational Biology 6: e1000667.Google ScholarPubMed
Wu, GD, Lewis, JD, Hoffmann, C, Chen, YY, Knight, R, Bittinger, K, Hwang, J, Chen, J, Berkowsky, R, Nessel, L, Li, H and Bushman, FD (2010). Sampling and pyrosequencing methods for characterizing bacterial communities in the human gut using 16S sequence tags. BMC Microbiology 10: 206.CrossRefGoogle ScholarPubMed
Yu, Z and Morrison, M (2004a). Comparisons of different hypervariable regions of rrs genes for use in fingerprinting of microbial communities by PCR-denaturing gradient gel electrophoresis. Applied and Environmental Microbiology 70: 48004806.CrossRefGoogle ScholarPubMed
Yu, Z and Morrison, M (2004b). Improved extraction of PCR-quality community DNA from digesta and fecal samples. Bio Techniques 36: 808812.Google ScholarPubMed
Yuan, S, Cohen, DB, Ravel, J, Abdo, Z and Forney, LJ (2012). Evaluation of methods for the extraction and purification of DNA from the human microbiome. Public Library of Science ONE 7: e33865.Google ScholarPubMed
Zhao, J, Li, J, Schloss, PD, Kalikin, LM, Raymond, TA, Petrosino, JF, Young, VB and Lipuma, JJ (2011). Effect of sample storage conditions on culture-independent bacterial community measures in cystic fibrosis sputum specimens. Journal of Clinical Microbiology 49: 37173718.CrossRefGoogle ScholarPubMed