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Abstract

Despite that obesity is associated with many metabolic diseases, a significant proportion (10–30 %) of obese individuals is recognized as ‘metabolically healthy obeses’ (MHOs). The aim of the current study is to characterize the gut microbiome for MHOs as compared to ‘metabolically unhealthy obeses’ (MUOs). We compared the gut microbiome of 172 MHO and 138 MUO individuals from Chongqing (China) (inclined to eat red meat and food with a spicy taste), and performed validation with selected biomarkers in 40 MHOs and 33 MUOs from Quanzhou (China) (inclined to eat seafood and food with a light/bland taste). The genera , and had increased abundance in both Chongqing and Quanzhou MHOs. We also observed different microbial functions in MUOs compared to MHOs, including an increased abundance of genes associated with glycan biosynthesis and metabolism. In addition, the microbial gene markers identified from the Chongqing cohort bear a moderate accuracy [AUC (area under the operating characteristic curve)=0.69] for classifying MHOs distinct from MUOs in the Quanzhou cohort. These findings indicate that gut microbiome is significantly distinct between MHOs and MUOs, implicating the potential of the gut microbiome in stratification and refined management of obesity.

Funding
This study was supported by the:
  • Sanming Project of Medicine in Shenzhen (Award SZSM202011016)
    • Principle Award Recipient: NotApplicable
  • National Key Clinical Specialty Discipline Construction Program of China (Award SZXK027)
    • Principle Award Recipient: NotApplicable
  • Shenzhen High-level Hospital Construction Fund (Award YBH2019-260)
    • Principle Award Recipient: NotApplicable
  • Military Healthcare Programs (Award 16BJZ40)
    • Principle Award Recipient: QiangZeng
  • Military Healthcare Programs (Award 15BJZ48)
    • Principle Award Recipient: QiangZeng
  • Natural Science Foundation of China (Award 81561128020)
    • Principle Award Recipient: QiangZeng
  • Natural Science Foundation of China (Award 81872920)
    • Principle Award Recipient: QiangZeng
  • Natural Science Foundation of China (Award 81602854)
    • Principle Award Recipient: QiangZeng
  • This is an open-access article distributed under the terms of the Creative Commons Attribution NonCommercial License.
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2021-08-06
2024-05-13
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References

  1. Tilg H, Kaser A. Gut microbiome, obesity, and metabolic dysfunction. J Clin Invest 2011; 121:2126–2132 [View Article] [PubMed]
    [Google Scholar]
  2. Despres JP, Lemieux I, Bergeron J, Pibarot P, Mathieu P et al. Abdominal obesity and the metabolic syndrome: contribution to global cardiometabolic risk. Arterioscler Thromb Vasc Biol 2008; 28:1039–1049 [View Article] [PubMed]
    [Google Scholar]
  3. Pindjakova J, Sartini C, Lo Re O, Rappa F, Coupe B et al. Gut dysbiosis and adaptive immune response in diet-induced obesity vs systemic inflammation. Front Microbiol 2017; 8:1157 [View Article] [PubMed]
    [Google Scholar]
  4. Muñoz-Garach A, Cornejo-Pareja I, Tinahones FJ. Does metabolically healthy obesity exist?. Nutrients 2016; 8:320 [View Article] [PubMed]
    [Google Scholar]
  5. Castaner O, Goday A, Park YM, Lee SH, Magkos F et al. The gut microbiome profile in obesity: A systematic review. Int J Endocrinol 2018; 2018:4095789 [View Article] [PubMed]
    [Google Scholar]
  6. Jumpertz R, Le DS, Turnbaugh PJ, Trinidad C, Bogardus C et al. Energy-balance studies reveal associations between gut microbes, caloric load, and nutrient absorption in humans. Am J Clin Nutr 2011; 94:58–65 [View Article] [PubMed]
    [Google Scholar]
  7. Faith JJ, Guruge JL, Charbonneau M, Subramanian S, Seedorf H et al. The long-term stability of the human gut microbiota. Science 2013; 341:1237439 [View Article] [PubMed]
    [Google Scholar]
  8. Guinane CM, Cotter PD. Role of the gut microbiota in health and chronic gastrointestinal disease: understanding a hidden metabolic organ. Therap Adv Gastroenterol 2013; 6:295–308 [View Article] [PubMed]
    [Google Scholar]
  9. Clarke G, Stilling RM, Kennedy PJ, Stanton C, Cryan JF et al. Minireview: gut microbiota: the neglected endocrine organ. Mol Endocrinol 2014; 28:1221–1238 [View Article] [PubMed]
    [Google Scholar]
  10. Furusawa Y, Obata Y, Fukuda S, Endo TA, Nakato G et al. Commensal microbe-derived butyrate induces the differentiation of colonic regulatory T cells. Nature 2013; 504:446–450 [View Article] [PubMed]
    [Google Scholar]
  11. Gérard P. Gut microbiome and obesity. How to prove causality?. Ann Am Thorac Soc 2017; 14:S354–S356 [View Article] [PubMed]
    [Google Scholar]
  12. Vallianou N, Stratigou T, Christodoulatos GS, Dalamaga M. Understanding the role of the gut microbiome and microbial metabolites in obesity and obesity-associated metabolic disorders: current evidence and perspectives. Curr Obes Rep 2019; 8:317–332 [View Article] [PubMed]
    [Google Scholar]
  13. Kasai C, Sugimoto K, Moritani I, Tanaka J, Oya Y et al. Comparison of the gut microbiota composition between obese and non-obese individuals in a Japanese population, as analyzed by terminal restriction fragment length polymorphism and next-generation sequencing. BMC Gastroenterol 2015; 15:100 [View Article] [PubMed]
    [Google Scholar]
  14. Moran-Ramos S, López-Contreras BE, Canizales-Quinteros S. Gut microbiota in obesity and metabolic abnormalities: a matter of composition or functionality?. Arch Med Res 2017; 48:735–753 [View Article] [PubMed]
    [Google Scholar]
  15. Schloss PD, Iverson KD, Petrosino JF, Schloss SJ. The dynamics of a family’s gut microbiota reveal variations on a theme. Microbiome 2014; 2:25 [View Article] [PubMed]
    [Google Scholar]
  16. Wen CP, Cheng TYD, Tsai SP, Chan HT, Hsu HL et al. Are Asians at greater mortality risks for being overweight than Caucasians? Redefining obesity for Asians. Public Health Nutr 2009; 12:497–506 [View Article] [PubMed]
    [Google Scholar]
  17. Chizyński K, Rózycka M. Hyperuricemia. Pol Merkur Lekarski 2005; 19:693–696 [PubMed]
    [Google Scholar]
  18. Goolsby MJ. National Kidney Foundation Guidelines for chronic kidney disease: evaluation, classification, and stratification. J Am Acad Nurse Pract 2002; 14:238–242 [View Article] [PubMed]
    [Google Scholar]
  19. Wagner Mackenzie B, Waite DW, Taylor MW. Evaluating variation in human gut microbiota profiles due to DNA extraction method and inter-subject differences. Front Microbiol 2015; 6:130 [View Article] [PubMed]
    [Google Scholar]
  20. Andrews S. FastQC: a quality control tool for high throughput sequence data. Babraham Institute, UK; 2014 www.bioinformatics.babraham.ac.uk/projects/fastqc
  21. Li H, Durbin R. Fast and accurate long-read alignment with Burrows-Wheeler transform. Bioinformatics 2010; 26:589–595 [View Article] [PubMed]
    [Google Scholar]
  22. Segata N, Waldron L, Ballarini A, Narasimhan V, Jousson O et al. Metagenomic microbial community profiling using unique clade-specific marker genes. Nat Methods 2012; 9:811–814 [View Article] [PubMed]
    [Google Scholar]
  23. Truong DT, Franzosa EA, Tickle TL, Scholz M, Weingart G et al. MetaPhlAn2 for enhanced metagenomic taxonomic profiling. Nat Methods 2015; 12:902–903 [View Article] [PubMed]
    [Google Scholar]
  24. Xie H, Guo R, Zhong H, Feng Q, Lan Z et al. Shotgun metagenomics of 250 adult twins reveals genetic and environmental impacts on the gut microbiome. Cell Syst 2016; 3:572–584 [View Article] [PubMed]
    [Google Scholar]
  25. Nielsen HB, Almeida M, Juncker AS, Rasmussen S, Li J et al. Identification and assembly of genomes and genetic elements in complex metagenomic samples without using reference genomes. Nat Biotechnol 2014; 32:822–828 [View Article] [PubMed]
    [Google Scholar]
  26. Qin J, Li Y, Cai Z, Li S, Zhu J et al. A metagenome-wide association study of gut microbiota in type 2 diabetes. Nature 2012; 490:55–60 [View Article] [PubMed]
    [Google Scholar]
  27. Benjamini Y, Hochberg Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc B 1995; 57:289–300 [View Article]
    [Google Scholar]
  28. Turnbaugh PJ, Hamady M, Yatsunenko T, Cantarel BL, Duncan A et al. A core gut microbiome in obese and lean twins. Nature 2009; 457:480–484 [View Article] [PubMed]
    [Google Scholar]
  29. Liu R, Hong J, Xu X, Feng Q, Zhang D et al. Gut microbiome and serum metabolome alterations in obesity and after weight-loss intervention. Nat Med 2017; 23:859–868 [View Article] [PubMed]
    [Google Scholar]
  30. John GK, Mullin GE. The gut microbiome and obesity. Curr Oncol Rep 2016; 18:45 [View Article] [PubMed]
    [Google Scholar]
  31. Lim MY, You HJ, Yoon HS, Kwon B, Lee JY et al. The effect of heritability and host genetics on the gut microbiota and metabolic syndrome. Gut 2017; 66:1031–1038 [View Article] [PubMed]
    [Google Scholar]
  32. Le Chatelier E, Nielsen T, Qin J, Prifti E, Hildebrand F et al. Richness of human gut microbiome correlates with metabolic markers. Nature 2013; 500:541–546 [View Article] [PubMed]
    [Google Scholar]
  33. Cotillard A, Kennedy SP, Kong LC, Prifti E, Pons N et al. Dietary intervention impact on gut microbial gene richness. Nature 2013; 500:585–588 [View Article] [PubMed]
    [Google Scholar]
  34. Thingholm LB, Rühlemann MC, Koch M, Fuqua B, Laucke G et al. Obese individuals with and without type 2 diabetes show different gut microbial functional capacity and composition. Cell Host Microbe 2019; 26:252–264 [View Article] [PubMed]
    [Google Scholar]
  35. Haro C, Garcia-Carpintero S, Alcala-Diaz JF, Gomez-Delgado F, Delgado-Lista J. The gut microbial community in metabolic syndrome patients is modified by diet. J Nutr Biochem 2016; 27:27–31 [View Article] [PubMed]
    [Google Scholar]
  36. Chaplin A, Carpéné C, Mercader J. Resveratrol, metabolic syndrome, and gut microbiota. Nutrients 2018; 10:1651 [View Article] [PubMed]
    [Google Scholar]
  37. Gerard P. Gut microbiota and obesity. Cell Mol Life Sci 2016; 73:147–162 [View Article] [PubMed]
    [Google Scholar]
  38. He Y, Wu W, Zheng HM, Li P, McDonald D et al. Regional variation limits applications of healthy gut microbiome reference ranges and disease models. Nat Med 2018; 24:1532–1535 [View Article] [PubMed]
    [Google Scholar]
  39. Rial SA, Karelis AD, Bergeron KF, Mounier C. Gut microbiota and metabolic health: the potential beneficial effects of a medium chain triglyceride diet in obese individuals. Nutrients 2016; 8:281 [View Article] [PubMed]
    [Google Scholar]
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