Abstract
The gut microbiota is crucial in the pathogenesis of type 2 diabetes mellitus (T2DM). However, the metabolism of T2DM patients is not well-understood. We aimed to identify the differences on composition and function of gut microbiota between T2DM patients with obesity and healthy people. In this study, 6 T2DM patients with obesity and 6 healthy volunteers were recruited, and metagenomic approach and bioinformatics analysis methods were used to understand the composition of the gut microbiota and the metabolic network. We found a decrease in the abundance of Firmicutes, Oribacterium, and Paenibacillus; this may be attributed to a possible mechanism and biological basis of T2DM; moreover, we identified three critical bacterial taxa, Bacteroides plebeius, Phascolarctobacterium sp. CAG207, and the order Acidaminococcales that can potentially be used for T2DM treatment. We also revealed the composition of the microbiota through functional annotation based on multiple databases and found that carbohydrate metabolism contributed greatly to the pathogenesis of T2DM. This study helps in elucidating the different metabolic roles of microbes in T2DM patients with obesity.
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References
Allen HJ, Kisailus EC (eds) (1992) Glycoconjugates : composition, structure, and function Dekker, New York, NY
American Diabetes Association (2018) 2. Classification and diagnosis of diabetes. Diabetes Care 41(Supplement 1):S13–S27. https://doi.org/10.2337/dc18-S002
Anbalagan R, Srikanth P, Mani M, Barani R, Seshadri KG, Janarthanan R (2017) Next generation sequencing of oral microbiota in type 2 diabetes mellitus prior to and after neem stick usage and correlation with serum monocyte chemoattractant-1. Diabetes Res Clin Pract 130:204–210. https://doi.org/10.1016/j.diabres.2017.06.009
Berlemont R, Martiny AC (2016) Glycoside hydrolases across environmental microbial communities. PLoS Comput Biol 12(12):e1005300. https://doi.org/10.1371/journal.pcbi.1005300
Buchfink B, Xie C, Huson DH (2015) Fast and sensitive protein alignment using diamond. Nat Methods 12(1):59–60. https://doi.org/10.1038/nmeth.3176
Campbell C, Adeolu M, Gupta RS (2015) Genome-based taxonomic framework for the class Negativicutes: division of the class negativicutes into the orders Selenomonadales emend., Acidaminococcales ord. nov. and Veillonellales ord. nov. Int J Syst Evol Microbiol 65(9):3203–3215. https://doi.org/10.1099/ijs.0.000347
Chinese Medical Association Diabetes Branch (2014) Chinese medical association diabetes branch. Guidelines for the prevention and treatment of type 2 diabetes in china. Peking University Medical Press, Beijing
Conlon MA, Bird AR (2014) The impact of diet and lifestyle on gut microbiota and human health. Nutrients 7(1):17–44. https://doi.org/10.3390/nu7010017
Di Bella JM, Bao Y, Gloor GB, Burton JP, Reid G (2013) High throughput sequencing methods and analysis for microbiome research. J Microbiol Methods 95(3):401–414. https://doi.org/10.1016/j.mimet.2013.08.011
Everard A, Lazarevic V, Gaïa N, Johansson M, Ståhlman M, Backhed F, Delzenne NM, Schrenzel J, François P, Cani PD (2014) Microbiome of prebiotic-treated mice reveals novel targets involved in host response during obesity. ISME J 8(10):2116–2130. https://doi.org/10.1038/ismej.2014.45
Gomes JMG, de Assis Costa J, de Cássia Gonçalves Alfenas R (2017) Metabolic endotoxemia and diabetes mellitus: a systematic review. Metabolism 68:133–144. https://doi.org/10.1016/j.metabol.2016.12.009
Guo J, Chen H, Song J, Wang J, Zhao L, Tong X (2014) Syndrome differentiation of diabetes by the traditional chinese medicine according to evidence-based medicine and expert consensus opinion. Evid Based Complement Alternat Med 2014:492193–492197. https://doi.org/10.1155/2014/492193
Ham B, Hwang HB, Jung SH, Chang S, Kang KD, Kwon MJ (2018) Distribution and diversity of ocular microbial communities in diabetic patients compared with healthy subjects. Curr Eye Res 43(3):314–324. https://doi.org/10.1080/02713683.2017.1406528
Hehemann JH, Correc G, Barbeyron T, Helbert W, Czjzek M, Michel G (2010) Transfer of carbohydrate-active enzymes from marine bacteria to japanese gut microbiota. Nature 464(7290):908–912. https://doi.org/10.1038/nature08937
Hollister EB, Gao C, Versalovic J (2014) Compositional and functional features of the gastrointestinal microbiome and their effects on human health. Gastroenterology 146(6):1449–1458. https://doi.org/10.1053/j.gastro.2014.01.052
IDF (2017) IDF diabetes atlas-8th edition. https://www.idf.org/e-library/epidemiology-research/diabetes-atlas/134-idf-diabetes-atlas-8th-edition.html. Accessed 25 Oct 2019
Larsen N, Vogensen FK, van den Berg FW, Nielsen DS, Andreasen AS, Pedersen BK, Al-Soud WA, Sorensen SJ, Hansen LH, Jakobsen M (2010) Gut microbiota in human adults with type 2 diabetes differs from non-diabetic adults. PLoS One 5(2):e9085. https://doi.org/10.1371/journal.pone.0009085
Li S, Li Y, Li W, Wang Z (2007) Investigation on characteristics of diabetic dampness heat syndrome and evolving regulation. J Hunan Univ Tradit Chin Med 27:65–68
Li H, Debowski AW, Liao T, Tang H, Nilsson HO, Marshall BJ, Stubbs KA, Benghezal M (2017) Understanding protein glycosylation pathways in bacteria. Future Microbiol 12:59–72. https://doi.org/10.2217/fmb-2016-0166
Liu D, Gao H, Tang W, Nie S (2017a) Plant non-starch polysaccharides that inhibit key enzymes linked to type 2 diabetes mellitus. Ann N Y Acad Sci 1401(1):28–36. https://doi.org/10.1111/nyas.13430
Liu F, Li P, Chen M, Luo Y, Prabhakar M, Zheng H, He Y, Qi Q, Long H, Zhang Y, Sheng H, Zhou H (2017b) Fructooligosaccharide (FOS) and galactooligosaccharide (GOS) increase Bifidobacterium but reduce butyrate producing bacteria with adverse glycemic metabolism in healthy young population. Sci Rep 7(1):11789. https://doi.org/10.1038/s41598-017-10722-2
Liu X, Li X, Shi Y, Wang L (2017c) Intervention study of tonifying qi and strengthening spleen method on intestinal flora in patients with type 2 diabetes. Liaoning J Tradit Chin Medicine 44(11):2311–2313
Martens EC, Koropatkin NM, Smith TJ, Gordon JI (2009) Complex glycan catabolism by the human gut microbiota: the Bacteroidetes sus-like paradigm. J Biol Chem 284(37):24673–24677. https://doi.org/10.1074/jbc.R109.022848
Nguyen VB, Nguyen AD, Wang SL (2017) Utilization of fishery processing by-product squid pens for alpha-glucosidase inhibitors production by Paenibacillus sp. Mar Drugs 15(9):274. https://doi.org/10.3390/md15090274
Noble D, Mathur R, Dent T, Meads C, Greenhalgh T (2011) Risk models and scores for type 2 diabetes: systematic review. BMJ 343:d7163. https://doi.org/10.1136/bmj.d7163
Samet JM (2013) Tobacco smoking: the leading cause of preventable disease worldwide. Thorac Surg Clin 23(2):103–112. https://doi.org/10.1016/j.thorsurg.2013.01.009
Santos-Marcos JA, Rangel-Zuniga OA, Jimenez-Lucena R, Quintana-Navarro GM, Garcia-Carpintero S, Malagon MM, Landa BB, Tena-Sempere M, Perez-Martinez P, Lopez-Miranda J, Perez-Jimenez F, Camargo A (2018) Influence of gender and menopausal status on gut microbiota. Maturitas 116:43–53. https://doi.org/10.1016/j.maturitas.2018.07.008
Schwiertz A (2016) Microbiota of the human body: implications in health and disease. Preface. Adv Exp Med Biol 902:1–3
Scott LJ, Mohlke KL, Bonnycastle LL, Willer CJ, Li Y, Duren WL, Erdos MR, Stringham HM, Chines PS, Jackson AU, Prokunina-Olsson L, Ding CJ, Swift AJ, Narisu N, Hu T, Pruim R, Xiao R, Li XY, Conneely KN, Riebow NL, Sprau AG, Tong M, White PP, Hetrick KN, Barnhart MW, Bark CW, Goldstein JL, Watkins L, Xiang F, Saramies J, Buchanan TA, Watanabe RM, Valle TT, Kinnunen L, Abecasis GR, Pugh EW, Doheny KF, Bergman RN, Tuomilehto J, Collins FS, Boehnke M (2007) A genome-wide association study of type 2 diabetes in finns detects multiple susceptibility variants. Science 316(5829):1341–1345. https://doi.org/10.1126/science.1142382
Society CD (2018) Guidelines for the prevention and treatment of type 2 diabetes in china (2017). Chin J Pract Int Med 38(04):292–344
Suarez Moya A (2017) Microbiome and next generation sequencing. Rev Esp Quimioter 30(5):305–311
van Wyk N, Drancourt M, Henrissat B, Kremer L (2017) Current perspectives on the families of glycoside hydrolases of Mycobacterium tuberculosis: their importance and prospects for assigning function to unknowns. Glycobiology 27(2):112–122. https://doi.org/10.1093/glycob/cww099
Wang C, Li J, Xue H, Li Y, Huang J, Mai J, Chen J, Cao J, Wu X, Guo D, Yu L, Gu D (2015a) Type 2 diabetes mellitus incidence in chinese: contributions of overweight and obesity. Diabetes Res Clin Pract 107(3):424–432. https://doi.org/10.1016/j.diabres.2014.09.059
Wang W, Zheng S, Li L, Yang Y, Liu Y, Wang A, Sharshov K, Li Y (2018) Comparative metagenomics of the gut microbiota in wild greylag geese (Anser anser) and ruddy shelducks (Tadorna ferruginea). MicrobiologyOpen 8(5):e00725. https://doi.org/10.1002/mbo3.725
Wang WL, Xu SY, Ren ZG, Tao L, Jiang JW, Zheng SS (2015b) Application of metagenomics in the human gut microbiome. World J Gastroenterol 21(3):803–814. https://doi.org/10.3748/wjg.v21.i3.803-814
Wang X, Xu X, Xia Y (2017) Further analysis reveals new gut microbiome markers of type 2 diabetes mellitus. Antonie Van Leeuwenhoek 110(3):445–453. https://doi.org/10.1007/s10482-016-0805-3
Yang G, Fan L, Tan J, Qi G, Zhang Y, Samet JM, Taylor CE, Becker K, Xu J (1999) Smoking in china: findings of the 1996 national prevalence survey. JAMA 282(13):1247–1253. https://doi.org/10.1001/jama.282.13.1247-1253
Zeevi D, Korem T, Godneva A, Bar N, Kurilshikov A, Lotan-Pompan M, Weinberger A, Fu J, Wijmenga C, Zhernakova A, Segal E (2019) Structural variation in the gut microbiome associates with host health. Nature 568(7750):43–48. https://doi.org/10.1038/s41586-019-1065-y
Zhang X, Fang Z, Zhang C, Xia H, Jie Z, Han X, Chen Y, Ji L (2017) Effects of acarbose on the gut microbiota of prediabetic patients: a randomized, double-blind, controlled crossover trial. Diabetes Ther 8(2):293–307. https://doi.org/10.1007/s13300-017-0226-y
Acknowledgments
We would like to thank Beijing Hepingli Hospital in helping recruit subjects.
Funding
This research was funded by the National Natural Science Foundation of China, grant number NSFC 81774171, Tangshan Science and Technology Innovation Team Training Program grant number 18130219A, and collaborative innovation project of Chaoyang District in Beijing grant number CYXC1719.
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This article contains studies with human participants, and this study was carried out according to the guidelines of the Declaration of Helsinki, and the study protocol was approved by the Ethical Committee of Beijing Hepingli Hospital with both written and verbal consent from the subjects of the study.
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Wang, TY., Zhang, XQ., Chen, AL. et al. A comparative study of microbial community and functions of type 2 diabetes mellitus patients with obesity and healthy people. Appl Microbiol Biotechnol 104, 7143–7153 (2020). https://doi.org/10.1007/s00253-020-10689-7
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DOI: https://doi.org/10.1007/s00253-020-10689-7