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BioMed Research International
Volume 2014, Article ID 906168, 10 pages
http://dx.doi.org/10.1155/2014/906168
Research Article

Systematic Analysis of the Association between Gut Flora and Obesity through High-Throughput Sequencing and Bioinformatics Approaches

1Institute of Bioinformatics and Systems Biology, National Chiao Tung University, Hsinchu 300, Taiwan
2Department of Obstetrics and Gynecology, Hsinchu Mackay Memorial Hospital, Hsinchu 300, Taiwan
3Mackay Medicine, Nursing and Management College, Taipei 104, Taiwan
4Department of Medicine, Mackay Medical College, New Taipei City 251, Taiwan
5Tseng Han-Chi General Hospital, Nantou 542, Taiwan
6Health GeneTech Corporation, Taoyuan 330, Taiwan
7Graduate Institute of Biomedical Informatics, Taipei Medical University, Taipei 110, Taiwan
8Department of Biological Science and Technology, National Chiao Tung University, Hsinchu 300, Taiwan
9Center for Bioinformatics Research, National Chiao Tung University, Hsinchu 300, Taiwan
10Department of Biomedical Science and Environmental Biology, Kaohsiung Medical University, Kaohsiung 807, Taiwan

Received 11 April 2014; Accepted 27 June 2014; Published 14 August 2014

Academic Editor: Li-Ching Wu

Copyright © 2014 Chih-Min Chiu et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. J. R. Goldsmith and R. B. Sartor, “The role of diet on intestinal microbiota metabolism: downstream impacts on host immune function and health, and therapeutic implications,” Journal of Gastroenterology, vol. 49, no. 5, pp. 785–798, 2014. View at Publisher · View at Google Scholar
  2. J. Chen, X. He, and J. Huang, “Diet effects in gut microbiome and obesity,” Journal of Food Science, vol. 79, no. 4, pp. R442–R451, 2014. View at Google Scholar
  3. O. O. Erejuwa, S. A. Sulaiman, and M. S. Wahab, “Modulation of gut microbiota in the management of metabolic disorders: the prospects and challenges,” International Journal of Molecular Sciences, vol. 15, no. 3, pp. 4158–4188, 2014. View at Google Scholar
  4. G. L. Hold, M. Smith, C. Grange, E. R. Watt, E. M. El-Omar, and I. Mukhopadhya, “Role of the gut microbiota in inflammatory bowel disease pathogenesis: what have we learnt in the past 10 years?” World Journal of Gastroenterology, vol. 20, no. 5, pp. 1192–1210, 2014. View at Google Scholar
  5. M. Arumugam, J. Raes, E. Pelletier et al., “Enterotypes of the human gut microbiome,” Nature, vol. 473, no. 7346, pp. 174–180, 2011. View at Publisher · View at Google Scholar · View at Scopus
  6. G. D. Wu, J. Chen, C. Hoffmann et al., “Linking long-term dietary patterns with gut microbial enterotypes,” Science, vol. 334, no. 6052, pp. 105–108, 2011. View at Publisher · View at Google Scholar · View at Scopus
  7. J. Peterson, S. Garges, M. Giovanni et al., “The NIH human microbiome project,” Genome Research, vol. 19, no. 12, pp. 2317–2323, 2009. View at Publisher · View at Google Scholar · View at Scopus
  8. J. Qin, Y. Li, Z. Cai et al., “A metagenome-wide association study of gut microbiota in type 2 diabetes,” Nature, vol. 490, no. 7418, pp. 55–60, 2012. View at Publisher · View at Google Scholar · View at Scopus
  9. F. H. Karlsson, V. Tremaroli, I. Nookaew et al., “Gut metagenome in European women with normal, impaired and diabetic glucose control,” Nature, vol. 498, no. 7452, pp. 99–103, 2013. View at Publisher · View at Google Scholar · View at Scopus
  10. X. Zhang, D. Shen, Z. Fang et al., “Human gut microbiota changes reveal the progression of glucose intolerance,” PLoS ONE, vol. 8, no. 8, Article ID e71108, 2013. View at Publisher · View at Google Scholar · View at Scopus
  11. F. Karlsson, V. Tremaroli, J. Nielsen, and F. Backhed, “Assessing the human gut microbiota in metabolic diseases,” Diabetes, vol. 62, no. 10, pp. 3341–3349, 2013. View at Google Scholar
  12. A. Lyra, T. Rinttilä, J. Nikkilä et al., “Diarrhoea-predominant irritable bowel syndrome distinguishable by 16S rRNA gene phylotype quantification,” World Journal of Gastroenterology, vol. 15, no. 47, pp. 5936–5945, 2009. View at Publisher · View at Google Scholar · View at Scopus
  13. S. O. Noor, K. Ridgway, L. Scovell et al., “Ulcerative colitis and irritable bowel patients exhibit distinct abnormalities of the gut microbiota,” BMC Gastroenterology, vol. 10, article 134, 2010. View at Publisher · View at Google Scholar · View at Scopus
  14. M. Rajilić-Stojanović, E. Biagi, H. G. H. J. Heilig et al., “Global and deep molecular analysis of microbiota signatures in fecal samples from patients with irritable bowel syndrome,” Gastroenterology, vol. 141, no. 5, pp. 1792–1801, 2011. View at Publisher · View at Google Scholar · View at Scopus
  15. Y. Zhu, T. Michelle Luo, C. Jobin, and H. A. Young, “Gut microbiota and probiotics in colon tumorigenesis,” Cancer Letters, vol. 309, no. 2, pp. 119–127, 2011. View at Publisher · View at Google Scholar · View at Scopus
  16. M. A. Hullar, A. N. Burnett-Hartman, and J. W. Lampe, “Gut microbes, diet, and cancer,” Cancer Treatment and Research, vol. 159, pp. 377–399, 2014. View at Google Scholar
  17. H. R. Hagland and K. Soreide, “Cellular metabolism in colorectal carcinogenesis: influence of lifestyle, gut microbiome and metabolic pathways,” Cancer Letters, 2014. View at Publisher · View at Google Scholar
  18. K. Korpela, H. J. Flint, A. M. Johnstone et al., “Gut microbiota signatures predict host and microbiota responses to dietary interventions in obese individuals,” PLoS One, vol. 9, no. 3, Article ID e90702, 2014. View at Google Scholar
  19. B. A. Swinburn, G. Sacks, K. D. Hall et al., “The global obesity pandemic: shaped by global drivers and local environments,” The Lancet, vol. 378, no. 9793, pp. 804–814, 2011. View at Publisher · View at Google Scholar · View at Scopus
  20. K. C. Portero McLellan, K. Wyne, E. T. Villagomez, and W. A. Hsueh, “Therapeutic interventions to reduce the risk of progression from prediabetes to type 2 diabetes mellitus,” Therapeutics and Clinical Risk Management, vol. 10, pp. 173–188, 2014. View at Google Scholar
  21. A. Everard and P. D. Cani, “Diabetes, obesity and gut microbiota,” Best Practice and Research: Clinical Gastroenterology, vol. 27, no. 1, pp. 73–83, 2013. View at Publisher · View at Google Scholar · View at Scopus
  22. J. A. Bell, M. Kivimaki, and M. Hamer, “Metabolically healthy obesity and risk of incident type 2 diabetes: a meta-analysis of prospective cohort studies,” Obesity Reviews, vol. 15, no. 6, pp. 504–515, 2014. View at Publisher · View at Google Scholar
  23. D. Nagakubo, M. Shirai, Y. Nakamura et al., “Prophylactic effects of the glucagon-like Peptide-1 analog liraglutide on hyperglycemia in a rat model of type 2 diabetes mellitus associated with chronic pancreatitis and obesity,” Comparative Medicine, vol. 64, no. 2, pp. 121–127, 2014. View at Google Scholar
  24. M. Kratz, T. Baars, and S. Guyenet, “The relationship between high-fat dairy consumption and obesity, cardiovascular, and metabolic disease,” European Journal of Nutrition, vol. 52, no. 1, pp. 1–24, 2013. View at Publisher · View at Google Scholar · View at Scopus
  25. G. M. Hinnouho, S. Czernichow, A. Dugravot et al., “Metabolically healthy obesity and the risk of cardiovascular disease and type 2 diabetes: The Whitehall II Cohort Study,” European Heart Journal, 2014. View at Publisher · View at Google Scholar
  26. K. A. Britton, J. M. Massaro, J. M. Murabito, B. E. Kreger, U. Hoffmann, and C. S. Fox, “Body fat distribution, incident cardiovascular disease, cancer, and all-cause mortality,” Journal of the American College of Cardiology, vol. 62, no. 10, pp. 921–925, 2013. View at Publisher · View at Google Scholar · View at Scopus
  27. E. E. Frezza, M. S. Wachtel, and M. Chiriva-Internati, “Influence of obesity on the risk of developing colon cancer,” Gut, vol. 55, no. 2, pp. 285–291, 2006. View at Publisher · View at Google Scholar · View at Scopus
  28. K. Nakamura, A. Hongo, J. Kodama, and Y. Hiramatsu, “Fat accumulation in adipose tissues as a risk factor for the development of endometrial cancer,” Oncology Reports, vol. 26, no. 1, pp. 65–71, 2011. View at Publisher · View at Google Scholar · View at Scopus
  29. M. Remely, E. Aumueller, D. Jahn, B. Hippe, H. Brath, and A. G. Haslberger, “Microbiota and epigenetic regulation of inflammatory mediators in type 2 diabetes and obesity,” Beneficial Microbes, vol. 5, no. 1, pp. 33–43, 2014. View at Google Scholar
  30. R. E. Ley, P. J. Turnbaugh, S. Klein, and J. I. Gordon, “Microbial ecology: human gut microbes associated with obesity,” Nature, vol. 444, no. 7122, pp. 1022–1023, 2006. View at Publisher · View at Google Scholar · View at Scopus
  31. J. Shen, M. S. Obin, and L. Zhao, “The gut microbiota, obesity and insulin resistance,” Molecular Aspects of Medicine, vol. 34, no. 1, pp. 39–58, 2013. View at Publisher · View at Google Scholar · View at Scopus
  32. M. Nieuwdorp, P. W. Gilijamse, N. Pai, and L. M. Kaplan, “Role of the microbiome in energy regulation and metabolism,” Gastroenterology, vol. 146, no. 6, pp. 1525–1533, 2014. View at Publisher · View at Google Scholar
  33. P. J. Turnbaugh, F. Bäckhed, L. Fulton, and J. I. Gordon, “Diet-induced obesity is linked to marked but reversible alterations in the mouse distal gut microbiome,” Cell Host and Microbe, vol. 3, no. 4, pp. 213–223, 2008. View at Publisher · View at Google Scholar · View at Scopus
  34. F. Bäckhed, H. Ding, T. Wang et al., “The gut microbiota as an environmental factor that regulates fat storage,” Proceedings of the National Academy of Sciences of the United States of America, vol. 101, no. 44, pp. 15718–15723, 2004. View at Publisher · View at Google Scholar · View at Scopus
  35. P. J. Turnbaugh, M. Hamady, T. Yatsunenko et al., “A core gut microbiome in obese and lean twins,” Nature, vol. 457, no. 7228, pp. 480–484, 2009. View at Publisher · View at Google Scholar · View at Scopus
  36. J. Furet, L. Kong, J. Tap et al., “Differential adaptation of human gut microbiota to bariatric surgery-induced weight loss: links with metabolic and low-grade inflammation markers,” Diabetes, vol. 59, no. 12, pp. 3049–3057, 2010. View at Publisher · View at Google Scholar · View at Scopus
  37. H. Zhang, J. K. DiBaise, A. Zuccolo et al., “Human gut microbiota in obesity and after gastric bypass,” Proceedings of the National Academy of Sciences of the United States of America, vol. 106, no. 7, pp. 2365–2370, 2009. View at Publisher · View at Google Scholar · View at Scopus
  38. Y. N. Yin, Q. F. Yu, N. Fu, X. W. Liu, and F. G. Lu, “Effects of four Bifidobacteria on obesity in high-fat diet induced rats,” World Journal of Gastroenterology, vol. 16, no. 27, pp. 3394–3401, 2010. View at Publisher · View at Google Scholar · View at Scopus
  39. R. E. Ley, “Obesity and the human microbiome,” Current Opinion in Gastroenterology, vol. 26, no. 1, pp. 5–11, 2010. View at Publisher · View at Google Scholar · View at Scopus
  40. The Human Microbiome Project Consortium, “Structure, function and diversity of the healthy human microbiome,” Nature, vol. 486, no. 7402, pp. 207–214, 2012. View at Publisher · View at Google Scholar
  41. W. Pan, K. M. Flegal, H. Chang, W. Yeh, C. Yeh, and W. Lee, “Body mass index and obesity-related metabolic disorders in Taiwanese and US whites and blacks: Implications for definitions of overweight and obesity for Asians,” The American Journal of Clinical Nutrition, vol. 79, no. 1, pp. 31–39, 2004. View at Google Scholar · View at Scopus
  42. A. Santacruz, M. C. Collado, L. García-Valdés et al., “Gut microbiota composition is associated with body weight, weight gain and biochemical parameters in pregnant women,” British Journal of Nutrition, vol. 104, no. 1, pp. 83–92, 2010. View at Publisher · View at Google Scholar · View at Scopus
  43. S. Xiao, N. Fei, X. Pang et al., “A gut microbiota-targeted dietary intervention for amelioration of chronic inflammation underlying metabolic syndrome,” FEMS Microbiology Ecology, vol. 87, no. 2, pp. 357–367, 2014. View at Google Scholar
  44. L. Rigsbee, R. Agans, V. Shankar et al., “Quantitative profiling of gut microbiota of children with diarrhea-predominant irritable bowel syndrome,” The American Journal of Gastroenterology, vol. 107, no. 11, pp. 1740–1751, 2012. View at Publisher · View at Google Scholar · View at Scopus
  45. N. Wu, X. Yang, R. Zhang et al., “Dysbiosis signature of fecal microbiota in colorectal cancer patients,” Microbial Ecology, vol. 66, no. 2, pp. 462–470, 2013. View at Publisher · View at Google Scholar · View at Scopus
  46. W. Chen, F. Liu, Z. Ling, X. Tong, and C. Xiang, “Human intestinal lumen and mucosa-associated microbiota in patients with colorectal cancer,” PLoS ONE, vol. 7, no. 6, Article ID e39743, 2012. View at Publisher · View at Google Scholar · View at Scopus
  47. Q. Zhu, Z. Jin, W. Wu et al., “Analysis of the intestinal lumen microbiota in an animal model of colorectal cancer,” PLoS ONE, vol. 9, no. 3, Article ID e90849, 2014. View at Google Scholar
  48. D. Wang, D. Yan, W. Hou, X. Zeng, Y. Qi, and J. Chen, “Characterization of blaOxA-23gene regions in isolates of Acinetobacter baumannii,” Journal of Microbiology, Immunology and Infection, 2014. View at Publisher · View at Google Scholar
  49. H. Urbanczyk, J. C. Ast, M. J. Higgins, J. Carson, and P. V. Dunlap, “Reclassification of Vibrio fischeri, Vibrio logei, Vibrio salmonicida and Vibrio wodanis as Aliivibrio fischeri gen. nov., comb. nov., Aliivibrio logei comb. nov., Aliivibrio salmonicida comb. nov. and Aliivibrio wodanis comb. nov,” International Journal of Systematic and Evolutionary Microbiology, vol. 57, part 12, pp. 2823–2829, 2007. View at Publisher · View at Google Scholar · View at Scopus
  50. J. C. Ast, H. Urbanczyk, and P. V. Dunlap, “Multi-gene analysis reveals previously unrecognized phylogenetic diversity in Aliivibrio,” Systematic and Applied Microbiology, vol. 32, no. 6, pp. 379–386, 2009. View at Publisher · View at Google Scholar · View at Scopus
  51. R. Beaz-Hidalgo, A. Doce, S. Balboa, J. L. Barja, and J. L. Romalde, “Aliivibrio finisterrensis sp. nov., isolated from Manila clam, Ruditapes philippinarum and emended description of the genus Aliivibrio,” International Journal of Systematic and Evolutionary Microbiology, vol. 60, no. 1, pp. 223–228, 2010. View at Publisher · View at Google Scholar · View at Scopus
  52. S. Yoshizawa, H. Karatani, M. Wada, A. Yokota, and K. Kogure, “Aliivibrio sifiae sp. nov., luminous marine bacteria isolated from seawater,” Journal of General and Applied Microbiology, vol. 56, no. 6, pp. 509–518, 2010. View at Publisher · View at Google Scholar · View at Scopus
  53. Y. S. Chen, Y. C. Liu, M. Y. Yen, J. H. Wang, S. R. Wann, and D. L. Cheng, “Skin and soft-tissue manifestations of Shewanella putrefaciens infection,” Clinical Infectious Diseases, vol. 25, no. 2, pp. 225–229, 1997. View at Publisher · View at Google Scholar · View at Scopus
  54. N. Vignier, M. Barreau, C. Olive et al., “Human infection with Shewanella putrefaciens and S. algae: report of 16 cases in Martinique and review of the literature,” American Journal of Tropical Medicine and Hygiene, vol. 89, no. 1, pp. 151–156, 2013. View at Publisher · View at Google Scholar · View at Scopus
  55. R. F. Boente, L. Q. Ferreira, L. S. Falcão et al., “Detection of resistance genes and susceptibility patterns in Bacteroides and Parabacteroides strains,” Anaerobe, vol. 16, no. 3, pp. 190–194, 2010. View at Publisher · View at Google Scholar · View at Scopus
  56. M. Sakamoto and Y. Benno, “Reclassification of Bacteroides distasonis, Bacteroides goldsteinii and Bacteroides merdae as Parabacteroides distasonis gen. nov., comb. nov., Parabacteroides goldsteinii comb. nov and Parabacteroides merdae comb. nov,” International Journal of Systematic and Evolutionary Microbiology, vol. 56, part 7, pp. 1599–1605, 2006. View at Publisher · View at Google Scholar · View at Scopus
  57. J. Xu, M. A. Mahowald, R. E. Ley et al., “Evolution of symbiotic bacteria in the distal human intestine.,” PLoS Biology, vol. 5, no. 7, Article ID e156, 2007. View at Publisher · View at Google Scholar · View at Scopus
  58. J. M. Clarke, D. L. Topping, C. T. Christophersen et al., “Butyrate esterified to starch is released in the human gastrointestinal tract,” The American Journal of Clinical Nutrition, vol. 94, no. 5, pp. 1276–1283, 2011. View at Publisher · View at Google Scholar · View at Scopus
  59. E. Sánchez, E. Donat, C. Ribes-Koninckx, M. Calabuig, and Y. Sanz, “Intestinal Bacteroides species associated with coeliac disease,” Journal of Clinical Pathology, vol. 63, no. 12, pp. 1105–1111, 2010. View at Publisher · View at Google Scholar · View at Scopus
  60. N. Becker, J. Kunath, G. Loh, and M. Blaut, “Human intestinal microbiota: characterization of a simplified and stable gnotobiotic rat model,” Gut Microbes, vol. 2, no. 1, 2011. View at Publisher · View at Google Scholar · View at Scopus
  61. N. Fei and L. Zhao, “An opportunistic pathogen isolated from the gut of an obese human causes obesity in germfree mice,” ISME Journal, vol. 7, no. 4, pp. 880–884, 2013. View at Publisher · View at Google Scholar · View at Scopus
  62. A. Hejazi and F. R. Falkiner, “Serratia marcescens,” Journal of Medical Microbiology, vol. 46, no. 11, pp. 903–912, 1997. View at Publisher · View at Google Scholar · View at Scopus
  63. M. Patankar, S. Sukumaran, A. Chhibba, U. Nayak, and L. Sequeira, “Comparative in-vitro activity of cefoperazone-tazobactam and cefoperazone-sulbactam combinations against ESBL pathogens in respiratory and urinary infections,” Journal of Association of Physicians of India, vol. 60, no. 11, pp. 22–24, 2012. View at Google Scholar · View at Scopus
  64. E. M. Carlisle, V. Poroyko, M. S. Caplan, J. Alverdy, M. J. Morowitz, and D. Liu, “Murine gut microbiota and transcriptome are diet dependent,” Annals of Surgery, vol. 257, no. 2, pp. 287–294, 2013. View at Publisher · View at Google Scholar · View at Scopus
  65. C. de Weerth, S. Fuentes, P. Puylaert, and W. M. de vos, “Intestinal microbiota of infants with colic: development and specific signatures,” Pediatrics, vol. 131, no. 2, pp. e550–e558, 2013. View at Publisher · View at Google Scholar · View at Scopus
  66. J. G. Caporaso, C. L. Lauber, W. A. Walters et al., “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, vol. 108, no. 1, pp. 4516–4522, 2011. View at Publisher · View at Google Scholar · View at Scopus
  67. E. Pruesse, C. Quast, K. Knittel et al., “SILVA: a comprehensive online resource for quality checked and aligned ribosomal RNA sequence data compatible with ARB,” Nucleic Acids Research, vol. 35, no. 21, pp. 7188–7196, 2007. View at Publisher · View at Google Scholar · View at Scopus
  68. R. C. Edgar, “Search and clustering orders of magnitude faster than BLAST,” Bioinformatics, vol. 26, no. 19, pp. 2460–2461, 2010. View at Publisher · View at Google Scholar · View at Scopus
  69. C. Lozupone, M. E. Lladser, D. Knights, J. Stombaugh, and R. Knight, “UniFrac: an effective distance metric for microbial community comparison,” ISME Journal, vol. 5, no. 2, pp. 169–172, 2011. View at Publisher · View at Google Scholar · View at Scopus
  70. M. Hall, E. Frank, G. Holmes, B. Pfahringer, P. Reutemann, and I. H. Witten, “The WEKA data mining software: an update,” SIGKDD Explorations, vol. 11, no. 1, pp. 10–18, 2009. View at Google Scholar