Microbiome in Human Health and Disease

Dr Ramana Madupu; Sebastian Szpakowski; Dr Karen E Nelson

doi:10.3184/003685013X13683759820813

. 2013 Jun 2;96(2):153–170. doi: 10.3184/003685013X13683759820813

Microbiome in Human Health and Disease

Ramana Madupu ^2,^✉, Sebastian Szpakowski ², Karen E Nelson ¹

¹J. Craig Venter Institute (JCVI) The J. Craig Venter Institute, 9704 Medical Center Drive, Rockville, MD 20850, USA.

²J. Craig Venter Institute.

Dr Nelson has extensive experience in microbial ecology, microbial genomics, microbial physiology and metagenomics. She has led several genomic and metagenomic efforts, and led the first published human metagenomics study in 2006. Ongoing studies in her group include metagenomic approaches to study the ecology of the gastrointestinal tract of humans and animals, studies on the relationship between the microbiome and various human and animal disease conditions, reference genome sequencing and analysis primarily for the human body, and other ‘omics’ studies. She has authored or co-authored over 100 peer reviewed publications and edited three books. She is standing member of the NRC Committee on Biodefense, a member of the National Academy of Sciences Board of Life Sciences, and Fellow of the American Academy of Microbiology.

Dr Madupu's research focuses on several human microbiome projects including omics analysis, survey of bacterial and viral species associated with the gut microbiome in Type 1 Diabetes, role of microbiota in esophageal adenocarcinoma and wound infections. She has lead efforts for bench marking and evaluation of annotation methods for reference genomes and metagenomic data for the Human Microbiome Project. Her research interests include genome annotation, interpretation and analysis of viral, microbial and metagenomes, tool development for genome analysis, process design and development of annotation pipelines, and improving gene annotation methods. She has co-authored several genome analysis papers and book chapters.

He received his PhD from Yale University in 2010. His PhD work included characterisation of epigenetic changes affecting mammalian transposable element and their contribution to cancer progression. The work built upon robust integration of large volumes of data and annotation, using relational databases and semantic web technologies. He currently analyses complex, high-throughput datasets in a number of metagenomics projects at the institute.

^✉

E-mail: rmadupu@jcvi.org

PMCID: PMC10365526 PMID: 23901633

Abstract

Metagenomic studies have truly revolutionised biology and medicine, and changed the way we study genomics. As genome sequencing becomes cheaper, it is being applied to study complex metagenomes. ‘Metagenome’ is the genetic material recovered directly from an environmental sample or niche. By delivering fast, cheap, and large volumes of data Next Generation Sequencing (NGS) platforms have facilitated a deeper understanding of the fundamentals of genomes, gene functions and regulation. Metagenomics, also referred to as environmental or community genomics, has brought about radical changes in our ability to analyse complex microbial communities by direct sampling of their natural habitat paving the way for the creation of innovative new areas for biomedical research. Many metagenomic studies involving the ‘human microbiome’ have been undertaken to date. Samples from of a number of diverse habitats including different human body sites have been subject to metagenomic examinations. Huge national and international projects with the purpose of elucidating the biogeography of microbial communities living within and on the human body, are well underway. The analysis of human microbiome data has brought about a paradigm shift in our understanding of the role of resident microflora in human health and disease and brings non-traditional areas such as gut ecology to the forefront of personalised medicine. In this chapter, we present an overview of the state-of-the-art in current literature and projects pertaining to human microbiome studies.

Keywords: microbiome, metagenome, biomarkers, genome sequencing, human health, omics

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References

1.Gill S. R. et al. (2006) Science, 312, 1355–1359. [DOI] [PMC free article] [PubMed] [Google Scholar]
2.The NIH HMP Working Group (2009) Genome Res., 19, 2317–2323. [DOI] [PMC free article] [PubMed] [Google Scholar]
3.Methé B.A. et al. (2012) Nature, 486, 215–221. [DOI] [PMC free article] [PubMed] [Google Scholar]
4.Huttenhower C. et al. (2012) Nature, 486, 207–214. [DOI] [PMC free article] [PubMed] [Google Scholar]
5.Aagaard K. et al. (2012) FASEB J., doi:10.1096/fj.12-220806. [Google Scholar]
6.Gevers D. et al. (2012) PLoS Biol., 10, e1001377. [DOI] [PMC free article] [PubMed] [Google Scholar]
7.Faust K. et al. (2012) PLoS Computat. Biol., 8, e1002606. [DOI] [PMC free article] [PubMed] [Google Scholar]
8.Qin J.L. R. et al. (2010) Nature, 464, 59–65. [DOI] [PMC free article] [PubMed] [Google Scholar]
9.Arumugam M. et al. (2011) Nature, 473, 174–180. [DOI] [PMC free article] [PubMed] [Google Scholar]
10.Koren O. et al. (2013) PLoS Comput. Biol., 9, e1002863. [DOI] [PMC free article] [PubMed] [Google Scholar]
11.Fouts D. E., Torralba M., Nelson K. E., Brenner D. A., and Schnabl B. (2012) J. Hepatol., 56, 1283–1292. [DOI] [PMC free article] [PubMed] [Google Scholar]
12.Yan A. W. et al. (2011) Hepatology, 53, 96–105. [DOI] [PMC free article] [PubMed] [Google Scholar]
13.Maga E. A., Weimer B. C., and Murray J. D. (2012) Gut microbes 4. [DOI] [PMC free article] [PubMed] [Google Scholar]
14.Jeong K., Nguyen V., and Kim J. (2012) BMB Rep., 45, 433–441. [DOI] [PubMed] [Google Scholar]
15.Dominguez-Bello M. G. et al. (2010) Proc. Natl. Acad. Sci. USA, 107, 11971–11975. [DOI] [PMC free article] [PubMed] [Google Scholar]
16.Murgas Torrazza R., and Neu J. (2011) J. Perinatol., 31 Suppl 1, S29–34. [DOI] [PubMed] [Google Scholar]
17.Lederberg J., and Mccray A. (2001) Ome Sweet ‘Omics'–A genealogical treasury of words. http://www.citeulike.org/group/13847/article/7659053.
18.O'Sullivan D.J.M. et al. (1960) J. Clin. Pathol., 13, 527. [DOI] [PMC free article] [PubMed] [Google Scholar]
19.Hugenholtz P., Goebel B. M., and Pace N. R. (1998) J. Bacter, 180, 4765–4774. [DOI] [PMC free article] [PubMed] [Google Scholar]
20.Amann R.I. et al. (1995) Microbiol. Rev., 59, 143. [DOI] [PMC free article] [PubMed] [Google Scholar]
21.Quail M. A. et al. (2012) BMC Genomics 13, 341. [DOI] [PMC free article] [PubMed] [Google Scholar]
22.Wooley J. C., Godzik A., and Friedberg I. (2010) PLoS Computat. Biol., 6, e1000667. [DOI] [PMC free article] [PubMed] [Google Scholar]
23.Handelsman J., Rondon M. R., Brady S. F., Clardy J., and Goodman R. M. (1998) Chem. Biol., 5, R245–249. [DOI] [PubMed] [Google Scholar]
24.Koonin E. V. (2003) Nature Rev. Microbiol., 1, 127–136. [DOI] [PubMed] [Google Scholar]
25.Koonin E. V. (2009) Int. J. Biochem. Cell Biol., 41, 298–306. [DOI] [PMC free article] [PubMed] [Google Scholar]
26.Xiong X., Boyett J. M., Webster R. G., and Stech J. (2009) J. Math. Biol., 59, 175–191. [DOI] [PMC free article] [PubMed] [Google Scholar]
27.DeLong E. F., and Pace N. R. (2001) System. Biol., 50, 470–478 (2001). [PubMed] [Google Scholar]
28.Woese C. R., and Fox G. E. (1977) Proc. Nat. Acad. Sci. USA, 74, 5088–5090. [DOI] [PMC free article] [PubMed] [Google Scholar]
29.Jumpstart Consortium Human Microbiome Project Data Generation Working Group (2012) PLoS ONE, 7, e0039315. [Google Scholar]
30.Huse S. M., Ye Y., Zhou Y., and Fodor A. A. (2012) PLoS ONE, 7, e34242. [DOI] [PMC free article] [PubMed] [Google Scholar]
31.Yatsunenko T. et al. (2012) Nature, 486, 222–227. [DOI] [PMC free article] [PubMed] [Google Scholar]
32.Wade W. G. (2012) Pharmacol. Res., 69, 137–143. [DOI] [PubMed] [Google Scholar]
33.Qin J. et al. (2010) Nature, 464, 59–65. [DOI] [PMC free article] [PubMed] [Google Scholar]
34.Klappenbach J. A., Dunbar J. M., and Schmidt T. M. (2000) Appl. Environ. Microbiol., 66, 1328–1333. [DOI] [PMC free article] [PubMed] [Google Scholar]
35.Klappenbach J. A., Saxman P. R., Cole J. R., and Schmidt T. M. (2001) Nucl. Acids Res., 29, 181–184. [DOI] [PMC free article] [PubMed] [Google Scholar]
36.Tringe S. G., and Hugenholtz P. (2008) Curr. Opin. Microbiol., 11, 442–446. [DOI] [PubMed] [Google Scholar]
37.Fouts D. E. et al. (2012) J. Trans. Med., 10, 174. [DOI] [PMC free article] [PubMed] [Google Scholar]
38.Gilles A. et al. (2011) BMC Genom., 12, 245. [DOI] [PMC free article] [PubMed] [Google Scholar]
39.Schloss P. D., Gevers D., and Westcott S. L. (2011) PLoS ONE, 6, e27310. [DOI] [PMC free article] [PubMed] [Google Scholar]
40.Quince C. (2011) BMC Bioinform., 12, 38. [DOI] [PMC free article] [PubMed] [Google Scholar]
41.Quince C. et al. (2009) Nature Meth., 6, 639–641. [DOI] [PubMed] [Google Scholar]
42.Niu B., Fu L., Sun S., and Li W. (2010) BMC Bioinform., 11, 187. [DOI] [PMC free article] [PubMed] [Google Scholar]
43.Chou H. H., and Holmes M. H. (2001) Bioinformatics, 17, 1093–1104. [DOI] [PubMed] [Google Scholar]
44.Haas B. J. (2011) Genome Res., 21, 494–504. [DOI] [PMC free article] [PubMed] [Google Scholar]
45.Edgar R. C., Haas B. J., Clemente J. C., Quince C., and Knight R. (2011) Bioinformatics, 27, 2194–2200. [DOI] [PMC free article] [PubMed] [Google Scholar]
46.Cole J.R.W.Q. (2009) Nucl. Acids Res., 37, D141–145 (2009). [DOI] [PMC free article] [PubMed] [Google Scholar]
47.Pruesse E. et al. (2007) Nucleic Acids Res., 35, 7188–7196. [DOI] [PMC free article] [PubMed] [Google Scholar]
48.Altschul S. F., Gish W., Miller W., Myers E. W., and Lipman D. J. (1990) Cell, 215, 403–410. [DOI] [PubMed] [Google Scholar]
49.Sun Y. et al. (2011) Brief. Bioinform., doi:10.1093/bib/bbr009. [Google Scholar]
50.DeSantis T. Z. et al. (2006) Nucl. Acids Res., 34, W394–W399. [DOI] [PMC free article] [PubMed] [Google Scholar]
51.Huber J. A. et al. (2009) Environ. Microbiol., 11, 1292–1302. [DOI] [PMC free article] [PubMed] [Google Scholar]
52.Larkin M. A. et al. (2007) Bioinformatics, 23, 2947–2948. [DOI] [PubMed] [Google Scholar]
53.Notredame C., Higgins D. G., and Heringa J. (2000) J. Molec. Biol., 302, 205–217. [DOI] [PubMed] [Google Scholar]
54.Sheneman L., Evans J., and Foster J. A. (2006) Bioinformatics, 22, 2823–2824. [DOI] [PubMed] [Google Scholar]
55.Tamura K. et al. (2011) Molec. Biol. Evolut., 28, 2731–2739. [DOI] [PMC free article] [PubMed] [Google Scholar]
56.Kim M., Morrison M., and Yu Z. (2011) J. Microbiol. Meth., 84, 81–87. [DOI] [PubMed] [Google Scholar]
57.Chakravorty S., Helb D., Burday M., Connell N., and Alland D. (2007) J. Microbiol. Meth., 69, 330–339. [DOI] [PMC free article] [PubMed] [Google Scholar]
58.Haas B. J. et al. (2011) Genome Res., 21, 494–504. [DOI] [PMC free article] [PubMed] [Google Scholar]
59.Lander E. S., and Waterman M. S. (1988) Genomics, 2, 231–239. [DOI] [PubMed] [Google Scholar]
60.Wendl M. C. (2006) J. Computat. Biol., 13, 1177–1196. [DOI] [PubMed] [Google Scholar]
61.Hooper S. D. et al. (2010) Bioinformatics, 26, 295–301. [DOI] [PMC free article] [PubMed] [Google Scholar]
62.Miller J. R., Koren S., and Sutton G. (2010) Genomics, 95, 315–327. [DOI] [PMC free article] [PubMed] [Google Scholar]
63.Paszkiewicz K., and Studholme D. J. (2010) Brief. Bioinform., 11, 457–472. [DOI] [PubMed] [Google Scholar]
64.Fleischmann R. D. et al. (1995) Science, 269, 496–512. [DOI] [PubMed] [Google Scholar]
65.Venter J. C. et al. (2001) Science, 291, 1304–1351. [DOI] [PubMed] [Google Scholar]
66.Kent W. J. (2002) Genome Res., 12, 656–664. [DOI] [PMC free article] [PubMed] [Google Scholar]
67.Li H., and Durbin R. (2009) Bioinformatics, 25, 1754–1760. [DOI] [PMC free article] [PubMed] [Google Scholar]
68.Langmead B., Trapnell C., Pop M., and Salzberg S. (2009) Genome Biol., 10, R25. [DOI] [PMC free article] [PubMed] [Google Scholar]
69.Haft D. H. et al. (2013) Nucl. Acids Res., 41, D387–395. [DOI] [PMC free article] [PubMed] [Google Scholar]
70.Huang Y., and Bystroff C. (2006) Bioinformatics, 22, 413–422. [DOI] [PubMed] [Google Scholar]
71.Siepel A. et al. (2005) Genome Res., 15, 1034–1050. [DOI] [PMC free article] [PubMed] [Google Scholar]
72.Johnson L. S., Eddy S. R., and Portugaly E. (2010) BMC Bioinform., 11, 431. [DOI] [PMC free article] [PubMed] [Google Scholar]
73.Brady A., and Salzberg S. (2011) Nature Meth., 8, 367. [DOI] [PMC free article] [PubMed] [Google Scholar]
74.Brady A., and Salzberg S. L. (2009) Nature Meth., 6, 673–676. [DOI] [PMC free article] [PubMed] [Google Scholar]
75.Liu B., Gibbons T., Ghodsi M., Treangen T., and Pop M. (2011) BMC Genom., 12 Suppl. 2, S4. [DOI] [PMC free article] [PubMed] [Google Scholar]
76.MacDonald N. J., Parks D. H., and Beiko R. G. (2012) Nucl. Acids Res., 40, e111. [DOI] [PMC free article] [PubMed] [Google Scholar]
77.Parks D. H., MacDonald N. J., and Beiko R. G. (2011) BMC Bioinform., 12, 328. [DOI] [PMC free article] [PubMed] [Google Scholar]
78.Rosen G. L., Polikar R., Caseiro D. A., Essinger S. D., and Sokhansanj B. A. (2011) J Biomed. Biotechnol., 2011, 495849. [DOI] [PMC free article] [PubMed] [Google Scholar]
79.Nelson K. E. et al. (2010) Science, 328, 994–999. [DOI] [PMC free article] [PubMed] [Google Scholar]
80.Goll J. et al. (2010) Bioinformatics, 26, 2631–2632. [DOI] [PMC free article] [PubMed] [Google Scholar]
81.McGrath K. C. et al. (2008) J. Microbiol. Meth., 75, 172–176. [DOI] [PubMed] [Google Scholar]
82.Gosalbes M. J. et al. (2011) PLoS ONE, 6, e17447. [DOI] [PMC free article] [PubMed] [Google Scholar]
83.Pérez-Cobas A. E. et al. (2012) Gut, doi:10.1136/gutjnl-2012-303184 (2012). [Google Scholar]
84.Zoetendal E. G. et al. (2012) ISME J., 6, 1415–1426. [DOI] [PMC free article] [PubMed] [Google Scholar]
85.Chen R. et al. (2012) Cell, 148, 1293–1307. [DOI] [PMC free article] [PubMed] [Google Scholar]
86.Chervonsky A. V. (2010) Nature Immunol., 11, 28–35. [DOI] [PubMed] [Google Scholar]
87.Munis L. R., Knosp C., and Yeretssian G. (2012) Front. Immunol., 3, 310. [DOI] [PMC free article] [PubMed] [Google Scholar]
88.Mychaleckyj J.C. et al. (2010) Clin Trials, 7, S75–S87. [DOI] [PMC free article] [PubMed] [Google Scholar]
89.McManus B. M. et al. (1993) Clin. Immunol. Immunopathol., 68, 159–169. [DOI] [PubMed] [Google Scholar]
90.Fairweather D., Kaya Z., Shellam G. R., Lawson C. M., and Rose N. R. (2001) J. Autoimmunol., 16, 175–186. [DOI] [PubMed] [Google Scholar]
91.Ercolini A. M., and Miller S. D. (2009) Clin. Exp. Immunol., 155, 1–15. [DOI] [PMC free article] [PubMed] [Google Scholar]
92.Cani P.D. (2007) Curr. Opin. Clin. Nutr. Metab. Care, 10, 729–734. [DOI] [PubMed] [Google Scholar]
93.Vrieze A. H. F., Zoetendal E.G., de Vos W.M., Hoekstra J.B., and Nieuwdorp M. (2010) Diabetologia, 53, 606–613. [DOI] [PMC free article] [PubMed] [Google Scholar]
94.Bell R.A., Beyer J.W., D'Agostino R.B. Jr., Lawrence J.M., Linder B., Liu L.L., Marcovina S.M., Rodriguez B.L., Williams D., and Dabelea D. (2009) Diabetes Care, 32, S102–111 (2009). [DOI] [PMC free article] [PubMed] [Google Scholar]
95.Gale E. A. M. T. (2002) Diabetes, 51, 3353–3361. [DOI] [PubMed] [Google Scholar]
96.Hurley D. (2009) Diabetes rising: how a rare disease became a modern pandemic, and what to do about it. Kaplan Publishing, Wokingham. [Google Scholar]
97.Lipton R.B. (2007) JAMA, 297, 2760–2762. [DOI] [PubMed] [Google Scholar]
98.Vehik K. H. R., Lezotte D., Norris J.M., Klingensmith G., Bloch C., Rewers M., and Dabelea D. (2007) Diabetes Care. 30, 503–509. [DOI] [PubMed] [Google Scholar]
99.Musso G., Gambino R., and Cassader M. (2010) Diabetes Care, 33, 2277–2284. [DOI] [PMC free article] [PubMed] [Google Scholar]
100.Hober D. S. F. (2010) Discov. Med., 10, 151–160. [PubMed] [Google Scholar]
101.Lammi N., Karvonen M., and Tuomilehto J. (2005) Med. Sci. Monit., 11, RA63–69. [PubMed] [Google Scholar]
102.Nenna R. et al. (2011) Int. J. Immunopathol. Pharmacol., 24, 651–659. [DOI] [PubMed] [Google Scholar]
103.Brain insulin resistance may exacerbate Alzheimer's progression. Researchers call it “Type III” diabetes. Duke Medicine Healthnews, 18, 4–5 (2012). [PubMed] [Google Scholar]
104.Tsai F., and Coyle W. J. (2009) Curr. Gastroenterol. Rep., 11, 307–313. [DOI] [PubMed] [Google Scholar]
105.Mitchell N. S., Catenacci V. A., Wyatt H. R., and Hill J. O. (2011) Psychiatr. Clin. N. Am., 34, 717–732. [DOI] [PMC free article] [PubMed] [Google Scholar]
106.Fernandez R., Miranda C., and Everett B. (2011) Int. J. Evidence-based healthcare, 9, 420–428. [DOI] [PubMed] [Google Scholar]
107.Hill J. O., Wyatt H. R., and Peters J. C. (2012) Circulation 126, 126–132. [DOI] [PMC free article] [PubMed] [Google Scholar]
108.Hyman M. A. (2006) Altern. Ther. Health Med., 12, 10–16. [PubMed] [Google Scholar]
109.Dongying Wu A. H. (2008) PLoS ONE, 3, e2566 (2008). [DOI] [PMC free article] [PubMed] [Google Scholar]
110.Carobbio S., Rodriguez-Cuenca S., and Vidal-Puig A. (2011) Curr. Opin. Clin. Nutrit. Metabol. Care, 14, 520–526. [DOI] [PubMed] [Google Scholar]
111.Turnbaugh P. J. et al. (2006) Nature, 444, 1027–1031. [DOI] [PubMed] [Google Scholar]
112.Velagapudi V. R. et al. (2010) J. Lipid Res., 51, 1101–1112. [DOI] [PMC free article] [PubMed] [Google Scholar]
113.Diamant M., Blaak E. E., and de Vos W. M. (2011) Obesity Rev., 12, 272–281. [DOI] [PubMed] [Google Scholar]
114.Caricilli A. M. et al. (2011) PLoS Biol, 9, e1001212. [DOI] [PMC free article] [PubMed] [Google Scholar] [Retracted]
115.Cani P. D. et al. (2009) Am. J. Clin. Nutrit., 90, 1236–1243. [DOI] [PubMed] [Google Scholar]
116.Ruiz A. G. et al. (2007) Obes. Surg., 17, 1374–1380. [DOI] [PubMed] [Google Scholar]
117.Nagpal R. et al. (2012) FEMS Microbiol. Lett., 334, 1–15. [DOI] [PubMed] [Google Scholar]
118.Raoult D. Nature Rev. Microbiol., 7, 616 (2009). [DOI] [PubMed] [Google Scholar]
119.Delzenne N., and Reid G. (2009) Nature Rev. Microbiol., 7, 901; author reply 901. [DOI] [PubMed] [Google Scholar]
120.Dai C. et al. (2013) Molec. Cell. Biochem., 374, 1–11. [DOI] [PubMed] [Google Scholar]
121.Calcinaro F. et al. (2005) Diabetologia, 48, 1565–1575. [DOI] [PubMed] [Google Scholar]
122.Ma X., Hua J., and Li Z. (2008) J. Hepatol., 49, 821–830. [DOI] [PMC free article] [PubMed] [Google Scholar]
123.Brandt L. J., and Reddy S. S. (2011) J. Clin. Gastroenterol., 45 Suppl, S159–167. [DOI] [PubMed] [Google Scholar]
124.Gough E., Shaikh H., and Manges A. R. (2011) Clin. Infect. Dis., 53, 994–1002. [DOI] [PubMed] [Google Scholar]
125.Petrof E.O. et al. (2013) Microbiome, 1(2013). [DOI] [PMC free article] [PubMed] [Google Scholar]

[bibr1-003685013X13683759820813] 1.Gill S. R. et al. (2006) Science, 312, 1355–1359. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bibr2-003685013X13683759820813] 2.The NIH HMP Working Group (2009) Genome Res., 19, 2317–2323. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bibr3-003685013X13683759820813] 3.Methé B.A. et al. (2012) Nature, 486, 215–221. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bibr4-003685013X13683759820813] 4.Huttenhower C. et al. (2012) Nature, 486, 207–214. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bibr5-003685013X13683759820813] 5.Aagaard K. et al. (2012) FASEB J., doi:10.1096/fj.12-220806. [Google Scholar]

[bibr6-003685013X13683759820813] 6.Gevers D. et al. (2012) PLoS Biol., 10, e1001377. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bibr7-003685013X13683759820813] 7.Faust K. et al. (2012) PLoS Computat. Biol., 8, e1002606. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bibr8-003685013X13683759820813] 8.Qin J.L. R. et al. (2010) Nature, 464, 59–65. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bibr9-003685013X13683759820813] 9.Arumugam M. et al. (2011) Nature, 473, 174–180. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bibr10-003685013X13683759820813] 10.Koren O. et al. (2013) PLoS Comput. Biol., 9, e1002863. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bibr11-003685013X13683759820813] 11.Fouts D. E., Torralba M., Nelson K. E., Brenner D. A., and Schnabl B. (2012) J. Hepatol., 56, 1283–1292. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bibr12-003685013X13683759820813] 12.Yan A. W. et al. (2011) Hepatology, 53, 96–105. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bibr13-003685013X13683759820813] 13.Maga E. A., Weimer B. C., and Murray J. D. (2012) Gut microbes 4. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bibr14-003685013X13683759820813] 14.Jeong K., Nguyen V., and Kim J. (2012) BMB Rep., 45, 433–441. [DOI] [PubMed] [Google Scholar]

[bibr15-003685013X13683759820813] 15.Dominguez-Bello M. G. et al. (2010) Proc. Natl. Acad. Sci. USA, 107, 11971–11975. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bibr16-003685013X13683759820813] 16.Murgas Torrazza R., and Neu J. (2011) J. Perinatol., 31 Suppl 1, S29–34. [DOI] [PubMed] [Google Scholar]

[bibr17-003685013X13683759820813] 17.Lederberg J., and Mccray A. (2001) Ome Sweet ‘Omics'–A genealogical treasury of words. http://www.citeulike.org/group/13847/article/7659053.

[bibr18-003685013X13683759820813] 18.O'Sullivan D.J.M. et al. (1960) J. Clin. Pathol., 13, 527. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bibr19-003685013X13683759820813] 19.Hugenholtz P., Goebel B. M., and Pace N. R. (1998) J. Bacter, 180, 4765–4774. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bibr20-003685013X13683759820813] 20.Amann R.I. et al. (1995) Microbiol. Rev., 59, 143. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bibr21-003685013X13683759820813] 21.Quail M. A. et al. (2012) BMC Genomics 13, 341. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bibr22-003685013X13683759820813] 22.Wooley J. C., Godzik A., and Friedberg I. (2010) PLoS Computat. Biol., 6, e1000667. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bibr23-003685013X13683759820813] 23.Handelsman J., Rondon M. R., Brady S. F., Clardy J., and Goodman R. M. (1998) Chem. Biol., 5, R245–249. [DOI] [PubMed] [Google Scholar]

[bibr24-003685013X13683759820813] 24.Koonin E. V. (2003) Nature Rev. Microbiol., 1, 127–136. [DOI] [PubMed] [Google Scholar]

[bibr25-003685013X13683759820813] 25.Koonin E. V. (2009) Int. J. Biochem. Cell Biol., 41, 298–306. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bibr26-003685013X13683759820813] 26.Xiong X., Boyett J. M., Webster R. G., and Stech J. (2009) J. Math. Biol., 59, 175–191. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bibr27-003685013X13683759820813] 27.DeLong E. F., and Pace N. R. (2001) System. Biol., 50, 470–478 (2001). [PubMed] [Google Scholar]

[bibr28-003685013X13683759820813] 28.Woese C. R., and Fox G. E. (1977) Proc. Nat. Acad. Sci. USA, 74, 5088–5090. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bibr29-003685013X13683759820813] 29.Jumpstart Consortium Human Microbiome Project Data Generation Working Group (2012) PLoS ONE, 7, e0039315. [Google Scholar]

[bibr30-003685013X13683759820813] 30.Huse S. M., Ye Y., Zhou Y., and Fodor A. A. (2012) PLoS ONE, 7, e34242. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bibr31-003685013X13683759820813] 31.Yatsunenko T. et al. (2012) Nature, 486, 222–227. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bibr32-003685013X13683759820813] 32.Wade W. G. (2012) Pharmacol. Res., 69, 137–143. [DOI] [PubMed] [Google Scholar]

[bibr33-003685013X13683759820813] 33.Qin J. et al. (2010) Nature, 464, 59–65. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bibr34-003685013X13683759820813] 34.Klappenbach J. A., Dunbar J. M., and Schmidt T. M. (2000) Appl. Environ. Microbiol., 66, 1328–1333. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bibr35-003685013X13683759820813] 35.Klappenbach J. A., Saxman P. R., Cole J. R., and Schmidt T. M. (2001) Nucl. Acids Res., 29, 181–184. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bibr36-003685013X13683759820813] 36.Tringe S. G., and Hugenholtz P. (2008) Curr. Opin. Microbiol., 11, 442–446. [DOI] [PubMed] [Google Scholar]

[bibr37-003685013X13683759820813] 37.Fouts D. E. et al. (2012) J. Trans. Med., 10, 174. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bibr38-003685013X13683759820813] 38.Gilles A. et al. (2011) BMC Genom., 12, 245. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bibr39-003685013X13683759820813] 39.Schloss P. D., Gevers D., and Westcott S. L. (2011) PLoS ONE, 6, e27310. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bibr40-003685013X13683759820813] 40.Quince C. (2011) BMC Bioinform., 12, 38. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bibr41-003685013X13683759820813] 41.Quince C. et al. (2009) Nature Meth., 6, 639–641. [DOI] [PubMed] [Google Scholar]

[bibr42-003685013X13683759820813] 42.Niu B., Fu L., Sun S., and Li W. (2010) BMC Bioinform., 11, 187. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bibr43-003685013X13683759820813] 43.Chou H. H., and Holmes M. H. (2001) Bioinformatics, 17, 1093–1104. [DOI] [PubMed] [Google Scholar]

[bibr44-003685013X13683759820813] 44.Haas B. J. (2011) Genome Res., 21, 494–504. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bibr45-003685013X13683759820813] 45.Edgar R. C., Haas B. J., Clemente J. C., Quince C., and Knight R. (2011) Bioinformatics, 27, 2194–2200. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bibr46-003685013X13683759820813] 46.Cole J.R.W.Q. (2009) Nucl. Acids Res., 37, D141–145 (2009). [DOI] [PMC free article] [PubMed] [Google Scholar]

[bibr47-003685013X13683759820813] 47.Pruesse E. et al. (2007) Nucleic Acids Res., 35, 7188–7196. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bibr48-003685013X13683759820813] 48.Altschul S. F., Gish W., Miller W., Myers E. W., and Lipman D. J. (1990) Cell, 215, 403–410. [DOI] [PubMed] [Google Scholar]

[bibr49-003685013X13683759820813] 49.Sun Y. et al. (2011) Brief. Bioinform., doi:10.1093/bib/bbr009. [Google Scholar]

[bibr50-003685013X13683759820813] 50.DeSantis T. Z. et al. (2006) Nucl. Acids Res., 34, W394–W399. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bibr51-003685013X13683759820813] 51.Huber J. A. et al. (2009) Environ. Microbiol., 11, 1292–1302. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bibr52-003685013X13683759820813] 52.Larkin M. A. et al. (2007) Bioinformatics, 23, 2947–2948. [DOI] [PubMed] [Google Scholar]

[bibr53-003685013X13683759820813] 53.Notredame C., Higgins D. G., and Heringa J. (2000) J. Molec. Biol., 302, 205–217. [DOI] [PubMed] [Google Scholar]

[bibr54-003685013X13683759820813] 54.Sheneman L., Evans J., and Foster J. A. (2006) Bioinformatics, 22, 2823–2824. [DOI] [PubMed] [Google Scholar]

[bibr55-003685013X13683759820813] 55.Tamura K. et al. (2011) Molec. Biol. Evolut., 28, 2731–2739. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bibr56-003685013X13683759820813] 56.Kim M., Morrison M., and Yu Z. (2011) J. Microbiol. Meth., 84, 81–87. [DOI] [PubMed] [Google Scholar]

[bibr57-003685013X13683759820813] 57.Chakravorty S., Helb D., Burday M., Connell N., and Alland D. (2007) J. Microbiol. Meth., 69, 330–339. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bibr58-003685013X13683759820813] 58.Haas B. J. et al. (2011) Genome Res., 21, 494–504. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bibr59-003685013X13683759820813] 59.Lander E. S., and Waterman M. S. (1988) Genomics, 2, 231–239. [DOI] [PubMed] [Google Scholar]

[bibr60-003685013X13683759820813] 60.Wendl M. C. (2006) J. Computat. Biol., 13, 1177–1196. [DOI] [PubMed] [Google Scholar]

[bibr61-003685013X13683759820813] 61.Hooper S. D. et al. (2010) Bioinformatics, 26, 295–301. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bibr62-003685013X13683759820813] 62.Miller J. R., Koren S., and Sutton G. (2010) Genomics, 95, 315–327. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bibr63-003685013X13683759820813] 63.Paszkiewicz K., and Studholme D. J. (2010) Brief. Bioinform., 11, 457–472. [DOI] [PubMed] [Google Scholar]

[bibr64-003685013X13683759820813] 64.Fleischmann R. D. et al. (1995) Science, 269, 496–512. [DOI] [PubMed] [Google Scholar]

[bibr65-003685013X13683759820813] 65.Venter J. C. et al. (2001) Science, 291, 1304–1351. [DOI] [PubMed] [Google Scholar]

[bibr66-003685013X13683759820813] 66.Kent W. J. (2002) Genome Res., 12, 656–664. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bibr67-003685013X13683759820813] 67.Li H., and Durbin R. (2009) Bioinformatics, 25, 1754–1760. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bibr68-003685013X13683759820813] 68.Langmead B., Trapnell C., Pop M., and Salzberg S. (2009) Genome Biol., 10, R25. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bibr69-003685013X13683759820813] 69.Haft D. H. et al. (2013) Nucl. Acids Res., 41, D387–395. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bibr70-003685013X13683759820813] 70.Huang Y., and Bystroff C. (2006) Bioinformatics, 22, 413–422. [DOI] [PubMed] [Google Scholar]

[bibr71-003685013X13683759820813] 71.Siepel A. et al. (2005) Genome Res., 15, 1034–1050. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bibr72-003685013X13683759820813] 72.Johnson L. S., Eddy S. R., and Portugaly E. (2010) BMC Bioinform., 11, 431. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bibr73-003685013X13683759820813] 73.Brady A., and Salzberg S. (2011) Nature Meth., 8, 367. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bibr74-003685013X13683759820813] 74.Brady A., and Salzberg S. L. (2009) Nature Meth., 6, 673–676. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bibr75-003685013X13683759820813] 75.Liu B., Gibbons T., Ghodsi M., Treangen T., and Pop M. (2011) BMC Genom., 12 Suppl. 2, S4. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bibr76-003685013X13683759820813] 76.MacDonald N. J., Parks D. H., and Beiko R. G. (2012) Nucl. Acids Res., 40, e111. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bibr77-003685013X13683759820813] 77.Parks D. H., MacDonald N. J., and Beiko R. G. (2011) BMC Bioinform., 12, 328. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bibr78-003685013X13683759820813] 78.Rosen G. L., Polikar R., Caseiro D. A., Essinger S. D., and Sokhansanj B. A. (2011) J Biomed. Biotechnol., 2011, 495849. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bibr79-003685013X13683759820813] 79.Nelson K. E. et al. (2010) Science, 328, 994–999. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bibr80-003685013X13683759820813] 80.Goll J. et al. (2010) Bioinformatics, 26, 2631–2632. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bibr81-003685013X13683759820813] 81.McGrath K. C. et al. (2008) J. Microbiol. Meth., 75, 172–176. [DOI] [PubMed] [Google Scholar]

[bibr82-003685013X13683759820813] 82.Gosalbes M. J. et al. (2011) PLoS ONE, 6, e17447. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bibr83-003685013X13683759820813] 83.Pérez-Cobas A. E. et al. (2012) Gut, doi:10.1136/gutjnl-2012-303184 (2012). [Google Scholar]

[bibr84-003685013X13683759820813] 84.Zoetendal E. G. et al. (2012) ISME J., 6, 1415–1426. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bibr85-003685013X13683759820813] 85.Chen R. et al. (2012) Cell, 148, 1293–1307. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bibr86-003685013X13683759820813] 86.Chervonsky A. V. (2010) Nature Immunol., 11, 28–35. [DOI] [PubMed] [Google Scholar]

[bibr87-003685013X13683759820813] 87.Munis L. R., Knosp C., and Yeretssian G. (2012) Front. Immunol., 3, 310. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bibr88-003685013X13683759820813] 88.Mychaleckyj J.C. et al. (2010) Clin Trials, 7, S75–S87. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bibr89-003685013X13683759820813] 89.McManus B. M. et al. (1993) Clin. Immunol. Immunopathol., 68, 159–169. [DOI] [PubMed] [Google Scholar]

[bibr90-003685013X13683759820813] 90.Fairweather D., Kaya Z., Shellam G. R., Lawson C. M., and Rose N. R. (2001) J. Autoimmunol., 16, 175–186. [DOI] [PubMed] [Google Scholar]

[bibr91-003685013X13683759820813] 91.Ercolini A. M., and Miller S. D. (2009) Clin. Exp. Immunol., 155, 1–15. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bibr92-003685013X13683759820813] 92.Cani P.D. (2007) Curr. Opin. Clin. Nutr. Metab. Care, 10, 729–734. [DOI] [PubMed] [Google Scholar]

[bibr93-003685013X13683759820813] 93.Vrieze A. H. F., Zoetendal E.G., de Vos W.M., Hoekstra J.B., and Nieuwdorp M. (2010) Diabetologia, 53, 606–613. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bibr94-003685013X13683759820813] 94.Bell R.A., Beyer J.W., D'Agostino R.B. Jr., Lawrence J.M., Linder B., Liu L.L., Marcovina S.M., Rodriguez B.L., Williams D., and Dabelea D. (2009) Diabetes Care, 32, S102–111 (2009). [DOI] [PMC free article] [PubMed] [Google Scholar]

[bibr95-003685013X13683759820813] 95.Gale E. A. M. T. (2002) Diabetes, 51, 3353–3361. [DOI] [PubMed] [Google Scholar]

[bibr96-003685013X13683759820813] 96.Hurley D. (2009) Diabetes rising: how a rare disease became a modern pandemic, and what to do about it. Kaplan Publishing, Wokingham. [Google Scholar]

[bibr97-003685013X13683759820813] 97.Lipton R.B. (2007) JAMA, 297, 2760–2762. [DOI] [PubMed] [Google Scholar]

[bibr98-003685013X13683759820813] 98.Vehik K. H. R., Lezotte D., Norris J.M., Klingensmith G., Bloch C., Rewers M., and Dabelea D. (2007) Diabetes Care. 30, 503–509. [DOI] [PubMed] [Google Scholar]

[bibr99-003685013X13683759820813] 99.Musso G., Gambino R., and Cassader M. (2010) Diabetes Care, 33, 2277–2284. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bibr100-003685013X13683759820813] 100.Hober D. S. F. (2010) Discov. Med., 10, 151–160. [PubMed] [Google Scholar]

[bibr101-003685013X13683759820813] 101.Lammi N., Karvonen M., and Tuomilehto J. (2005) Med. Sci. Monit., 11, RA63–69. [PubMed] [Google Scholar]

[bibr102-003685013X13683759820813] 102.Nenna R. et al. (2011) Int. J. Immunopathol. Pharmacol., 24, 651–659. [DOI] [PubMed] [Google Scholar]

[bibr103-003685013X13683759820813] 103.Brain insulin resistance may exacerbate Alzheimer's progression. Researchers call it “Type III” diabetes. Duke Medicine Healthnews, 18, 4–5 (2012). [PubMed] [Google Scholar]

[bibr104-003685013X13683759820813] 104.Tsai F., and Coyle W. J. (2009) Curr. Gastroenterol. Rep., 11, 307–313. [DOI] [PubMed] [Google Scholar]

[bibr105-003685013X13683759820813] 105.Mitchell N. S., Catenacci V. A., Wyatt H. R., and Hill J. O. (2011) Psychiatr. Clin. N. Am., 34, 717–732. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bibr106-003685013X13683759820813] 106.Fernandez R., Miranda C., and Everett B. (2011) Int. J. Evidence-based healthcare, 9, 420–428. [DOI] [PubMed] [Google Scholar]

[bibr107-003685013X13683759820813] 107.Hill J. O., Wyatt H. R., and Peters J. C. (2012) Circulation 126, 126–132. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bibr108-003685013X13683759820813] 108.Hyman M. A. (2006) Altern. Ther. Health Med., 12, 10–16. [PubMed] [Google Scholar]

[bibr109-003685013X13683759820813] 109.Dongying Wu A. H. (2008) PLoS ONE, 3, e2566 (2008). [DOI] [PMC free article] [PubMed] [Google Scholar]

[bibr110-003685013X13683759820813] 110.Carobbio S., Rodriguez-Cuenca S., and Vidal-Puig A. (2011) Curr. Opin. Clin. Nutrit. Metabol. Care, 14, 520–526. [DOI] [PubMed] [Google Scholar]

[bibr111-003685013X13683759820813] 111.Turnbaugh P. J. et al. (2006) Nature, 444, 1027–1031. [DOI] [PubMed] [Google Scholar]

[bibr112-003685013X13683759820813] 112.Velagapudi V. R. et al. (2010) J. Lipid Res., 51, 1101–1112. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bibr113-003685013X13683759820813] 113.Diamant M., Blaak E. E., and de Vos W. M. (2011) Obesity Rev., 12, 272–281. [DOI] [PubMed] [Google Scholar]

[bibr114-003685013X13683759820813] 114.Caricilli A. M. et al. (2011) PLoS Biol, 9, e1001212. [DOI] [PMC free article] [PubMed] [Google Scholar] [Retracted]

[bibr115-003685013X13683759820813] 115.Cani P. D. et al. (2009) Am. J. Clin. Nutrit., 90, 1236–1243. [DOI] [PubMed] [Google Scholar]

[bibr116-003685013X13683759820813] 116.Ruiz A. G. et al. (2007) Obes. Surg., 17, 1374–1380. [DOI] [PubMed] [Google Scholar]

[bibr117-003685013X13683759820813] 117.Nagpal R. et al. (2012) FEMS Microbiol. Lett., 334, 1–15. [DOI] [PubMed] [Google Scholar]

[bibr118-003685013X13683759820813] 118.Raoult D. Nature Rev. Microbiol., 7, 616 (2009). [DOI] [PubMed] [Google Scholar]

[bibr119-003685013X13683759820813] 119.Delzenne N., and Reid G. (2009) Nature Rev. Microbiol., 7, 901; author reply 901. [DOI] [PubMed] [Google Scholar]

[bibr120-003685013X13683759820813] 120.Dai C. et al. (2013) Molec. Cell. Biochem., 374, 1–11. [DOI] [PubMed] [Google Scholar]

[bibr121-003685013X13683759820813] 121.Calcinaro F. et al. (2005) Diabetologia, 48, 1565–1575. [DOI] [PubMed] [Google Scholar]

[bibr122-003685013X13683759820813] 122.Ma X., Hua J., and Li Z. (2008) J. Hepatol., 49, 821–830. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bibr123-003685013X13683759820813] 123.Brandt L. J., and Reddy S. S. (2011) J. Clin. Gastroenterol., 45 Suppl, S159–167. [DOI] [PubMed] [Google Scholar]

[bibr124-003685013X13683759820813] 124.Gough E., Shaikh H., and Manges A. R. (2011) Clin. Infect. Dis., 53, 994–1002. [DOI] [PubMed] [Google Scholar]

[bibr125-003685013X13683759820813] 125.Petrof E.O. et al. (2013) Microbiome, 1(2013). [DOI] [PMC free article] [PubMed] [Google Scholar]

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Microbiome in Human Health and Disease

Dr Ramana Madupu

Sebastian Szpakowski

Dr Karen E Nelson

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Microbiome in Human Health and Disease

Dr Ramana Madupu

Sebastian Szpakowski

Dr Karen E Nelson

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