Advertisement

Connection between gut microbiome and the development of obesity

  • Cuiting Zhi
  • Jingqing Huang
  • Jin Wang
  • Hua Cao
  • Yan Bai
  • Jiao GuoEmail author
  • Zhengquan SuEmail author
Review

Abstract

The potential role of the gut microbiota in various human diseases has attracted considerable attention worldwide. Here, we discuss the vital role of the intestinal microbiota in the development of obesity. First, we describe how the gut microbiota promotes fat accumulation. Additionally, a high-fat diet leads to structural instability among in the gut microbiota, further leading to an increase in endotoxins, which aggravates obesity. We then discuss how gut microbiota metabolites, including short-chain fatty acids and lipopolysaccharides, affect the host. Finally, we review several strategies for regulating the intestinal flora.

Keywords

Obesity Gut microbiota Fat accumulation LPS SCFAs Strategies 

Abbreviations

LPS

lipopolysaccharides

TNF-α

tumor necrosis factor-α

IL-1β

interleukin 1β

LPL

lipoprotein lipase

AMPK

adenosine monophosphate–activated protein kinase

SCFAs

short-chain fatty acids

FIAF

fasting-induced adipocyte factor

Cpt1

carnitine palmitoyl transferase-1

GPCRs

G protein–coupled receptors

TLR

Toll-like receptor

GLP

glucagon-like peptide

CD

clusters of differentiation

PGC-1α

receptor-gamma coactivator-1α

UCP-1

mitochondrial uncoupling protein-1

PYY

peptide YY

HFD

high-fat diet

TCA cycle

tricarboxylic acid cycle

LCFAs

long-chain fatty acids

Th.

T helper

Notes

Authors’ contributions

Cuiting Zhi had the idea for the article and drafted it. Jingqing Huang and Jin Wang performed the literature search. Cuiting Zhi, Yan Bai, Jiao Guo, and Zhengquan Su critically revised the work.

Funding information

This work was financially supported by the Industry University Research Collaborative Innovation Major Projects of Guangzhou Science Technology Innovation Commission, China (201604020164), Guangdong Provincial University Engineering Technology Research Center of Natural Products and Drugs (2017GCZX002), Technology Planning Project of Guangzhou, China (201806040009, 201804010349, 201804010329), and the National Science Foundation of China (no. 81173107).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. 1.
    Williams EP, Mesidor M, Winters K, Dubbert PM, Wyatt SB (2015) Overweight and obesity: prevalence, consequences, and causes of a growing public health problem. Curr Obes Rep 4(3):363–370.  https://doi.org/10.1007/s13679-015-0169-4 Google Scholar
  2. 2.
    Cani PD, Osto M, Geurts L, Everard A (2012) Involvement of gut microbiota in the development of low-grade inflammation and type 2 diabetes associated with obesity. Gut Microbes 3(4):279–288.  https://doi.org/10.4161/gmic.19625 Google Scholar
  3. 3.
    Carvalho BM, Guadagnini D, Tsukumo DML, Schenka AA, Latuf-Filho P, Vassallo J, Dias JC, Kubota LT, Carvalheira JBC, Saad MJA (2012) Modulation of gut microbiota by antibiotics improves insulin signalling in high-fat fed mice. Diabetologia 55(10):2823–2834.  https://doi.org/10.1007/s00125-012-2648-4 Google Scholar
  4. 4.
    Guarner F, Malagelada J-R (2003) Gut flora in health and disease. Lancet 361(9356):512–519.  https://doi.org/10.1016/s0140-6736(03)12489-0 Google Scholar
  5. 5.
    Eckburg PB, Bik EM, Bernstein CN, Purdom E, Dethlefsen L, Sargent M, Gill SR, Nelson KE, Relman DA (2005) Diversity of the human intestinal microbial flora. Science 308(5728):1635–1638.  https://doi.org/10.1126/science.1110591 Google Scholar
  6. 6.
    James SL, Muir JG, Curtis SL, Gibson PR (2003) Dietary fibre: a roughage guide. Intern Med J 33(7):291–296Google Scholar
  7. 7.
    Piya MK, Harte AL, McTernan PG (2013) Metabolic endotoxaemia: is it more than just a gut feeling? Curr Opin Lipidol 24(1):78–85.  https://doi.org/10.1097/MOL.0b013e32835b4431 Google Scholar
  8. 8.
    Teixeira TF, Collado MC, Ferreira CL, Bressan J, Peluzio Mdo C (2012) Potential mechanisms for the emerging link between obesity and increased intestinal permeability. Nutr Res 32(9):637–647.  https://doi.org/10.1016/j.nutres.2012.07.003 Google Scholar
  9. 9.
    Nieto-Vazquez I, Fernandez-Veledo S, Kramer DK, Vila-Bedmar R, Garcia-Guerra L, Lorenzo M (2008) Insulin resistance associated to obesity: the link TNF-alpha. Arch Physiol Biochem 114(3):183–194.  https://doi.org/10.1080/13813450802181047 Google Scholar
  10. 10.
    Zhao L (2013) The gut microbiota and obesity: from correlation to causality. Nat Rev Microbiol 11(9):639–647.  https://doi.org/10.1038/nrmicro3089 Google Scholar
  11. 11.
    Tabatabaei-Malazy O, Hasani-Ranjbar S, Amoli MM, Heshmat R, Sajadi M, Derakhshan R, Amiri P, Namakchian M, Rezazadeh E, Tavakkoly-Bazzaz J, Keshtkar A, Larijani B (2010) Gender-specific differences in the association of adiponectin gene polymorphisms with body mass index. Rev Diab Stud : RDS 7(3):241–246.  https://doi.org/10.1900/rds.2010.7.241 Google Scholar
  12. 12.
    Tavakkoly Bazzaz J, Shojapoor M, Nazem H, Amiri P, Fakhrzadeh H, Heshmat R, Parvizi M, Hasani Ranjbar S, Amoli MM (2010) Methylenetetrahydrofolate reductase gene polymorphism in diabetes and obesity. Mol Biol Rep 37(1):105–109.  https://doi.org/10.1007/s11033-009-9545-z Google Scholar
  13. 13.
    Ramdas M, Harel C, Armoni M, Karnieli E (2015) AHNAK KO mice are protected from diet-induced obesity but are glucose intolerant. Hormone Metab Res = Hormon- und Stoffwechselforschung = Hormones et metabolisme 47(4):265–272.  https://doi.org/10.1055/s-0034-1387736 Google Scholar
  14. 14.
    Moreno-Indias I, Cardona F, Tinahones FJ, Queipo-Ortuno MI (2014) Impact of the gut microbiota on the development of obesity and type 2 diabetes mellitus. Front Microbiol 5:190.  https://doi.org/10.3389/fmicb.2014.00190 Google Scholar
  15. 15.
    Turnbaugh PJ, Ley RE, Mahowald MA, Magrini V, Mardis ER, Gordon JI (2006) An obesity-associated gut microbiome with increased capacity for energy harvest. Nature 444(7122):1027–1031.  https://doi.org/10.1038/nature05414 Google Scholar
  16. 16.
    Ley RE, Backhed F, Turnbaugh P, Lozupone CA, Knight RD, Gordon JI (2005) Obesity alters gut microbial ecology. Proc Natl Acad Sci U S A 102(31):11070–11075.  https://doi.org/10.1073/pnas.0504978102 Google Scholar
  17. 17.
    Heimann E, Nyman M, Degerman E (2015) Propionic acid and butyric acid inhibit lipolysis and de novo lipogenesis and increase insulin-stimulated glucose uptake in primary rat adipocytes. Adipocyte 4(2):81–88.  https://doi.org/10.4161/21623945.2014.960694 Google Scholar
  18. 18.
    Chimerel C, Emery E, Summers DK, Keyser U, Gribble FM, Reimann F (2014) Bacterial metabolite indole modulates incretin secretion from intestinal enteroendocrine L cells. Cell Rep 9(4):1202–1208.  https://doi.org/10.1016/j.celrep.2014.10.032 Google Scholar
  19. 19.
    Backhed F, Ding H, Wang T, Hooper LV, Koh GY, Nagy A, Semenkovich CF, Gordon JI (2004) The gut microbiota as an environmental factor that regulates fat storage. Proc Natl Acad Sci U S A 101(44):15718–15723.  https://doi.org/10.1073/pnas.0407076101 Google Scholar
  20. 20.
    Backhed F, Manchester JK, Semenkovich CF, Gordon JI (2007) Mechanisms underlying the resistance to diet-induced obesity in germ-free mice. Proc Natl Acad Sci U S A 104(3):979–984.  https://doi.org/10.1073/pnas.0605374104 Google Scholar
  21. 21.
    Matsuo K, Matsusue K, Aibara D, Takiguchi S, Gonzalez FJ, Yamano S (2017) Insulin represses fasting-induced expression of hepatic fat-specific protein 27. Pharm Soc Japn 40(6):888–893Google Scholar
  22. 22.
    Hardie DG, Ross FA, Hawley SA (2012) AMPK: a nutrient and energy sensor that maintains energy homeostasis. Nat Rev Mol Cell Biol 13(4):251–262.  https://doi.org/10.1038/nrm3311 Google Scholar
  23. 23.
    Kahn BB, Alquier T, Carling D, Hardie DG (2005) AMP-activated protein kinase: ancient energy gauge provides clues to modern understanding of metabolism. Cell Metab 1(1):15–25.  https://doi.org/10.1016/j.cmet.2004.12.003 Google Scholar
  24. 24.
    Le Poul E, Loison C, Struyf S, Springael JY, Lannoy V, Decobecq ME, Brezillon S, Dupriez V, Vassart G, Van Damme J, Parmentier M, Detheux M (2003) Functional characterization of human receptors for short chain fatty acids and their role in polymorphonuclear cell activation. J Biol Chem 278(28):25481–25489.  https://doi.org/10.1074/jbc.M301403200 Google Scholar
  25. 25.
    Samuel BS, Shaito A, Motoike T, Rey FE, Backhed F, Manchester JK, Hammer RE, Williams SC, Crowley J, Yanagisawa M, Gordon JI (2008) Effects of the gut microbiota on host adiposity are modulated by the short-chain fatty-acid binding G protein-coupled receptor, Gpr41. Proc Natl Acad Sci U S A 105(43):16767–16772.  https://doi.org/10.1073/pnas.0808567105 Google Scholar
  26. 26.
    Karra E, Chandarana K, Batterham RL (2009) The role of peptide YY in appetite regulation and obesity. J Physiol 587(1):19–25.  https://doi.org/10.1113/jphysiol.2008.164269 Google Scholar
  27. 27.
    McNeil NI (1984) The contribution of the large intestine to energy supplies in man. Am J Clin Nutr 39(2):338–342.  https://doi.org/10.1093/ajcn/39.2.338 Google Scholar
  28. 28.
    Popovich DG, Jenkins DJ, Kendall CW, Dierenfeld ES, Carroll RW, Tariq N, Vidgen E (1997) The western lowland gorilla diet has implications for the health of humans and other hominoids. J Nutr 127(10):2000–2005.  https://doi.org/10.1093/jn/127.10.2000 Google Scholar
  29. 29.
    Frost GS, Walton GE, Swann JR, Psichas A, Costabile A, Johnson LP, Sponheimer M, Gibson GR, Barraclough TG (2014) Impacts of plant-based foods in ancestral hominin diets on the metabolism and function of gut microbiota in vitro. mBio 5(3):e00853–e00814.  https://doi.org/10.1128/mBio.00853-14 Google Scholar
  30. 30.
    Cummings JH, Pomare EW, Branch WJ, Naylor CP, Macfarlane GT (1987) Short chain fatty acids in human large intestine, portal, hepatic and venous blood. Gut 28(10):1221–1227Google Scholar
  31. 31.
    Levrat MA, Remesy C, Demigne C (1991) High propionic acid fermentations and mineral accumulation in the cecum of rats adapted to different levels of inulin. J Nutr 121(11):1730–1737.  https://doi.org/10.1093/jn/121.11.1730 Google Scholar
  32. 32.
    Donohoe DR, Garge N, Zhang X, Sun W, O’Connell TM, Bunger MK, Bultman SJ (2011) The microbiome and butyrate regulate energy metabolism and autophagy in the mammalian colon. Cell Metab 13(5):517–526.  https://doi.org/10.1016/j.cmet.2011.02.018 Google Scholar
  33. 33.
    De Vadder F, Kovatcheva-Datchary P, Goncalves D, Vinera J, Zitoun C, Duchampt A, Backhed F, Mithieux G (2014) Microbiota-generated metabolites promote metabolic benefits via gut-brain neural circuits. Cell 156(1–2):84–96.  https://doi.org/10.1016/j.cell.2013.12.016 Google Scholar
  34. 34.
    Frost G, Sleeth ML, Sahuri-Arisoylu M, Lizarbe B, Cerdan S, Brody L, Anastasovska J, Ghourab S, Hankir M, Zhang S, Carling D, Swann JR, Gibson G, Viardot A, Morrison D, Louise Thomas E, Bell JD (2014) The short-chain fatty acid acetate reduces appetite via a central homeostatic mechanism. Nat Commun 5:3611.  https://doi.org/10.1038/ncomms4611 Google Scholar
  35. 35.
    Blad CC, Tang C, Offermanns S (2012) G protein-coupled receptors for energy metabolites as new therapeutic targets. Nat Rev Drug Discov 11(8):603–619.  https://doi.org/10.1038/nrd3777 Google Scholar
  36. 36.
    Offermanns S (2014) Free fatty acid (FFA) and hydroxy carboxylic acid (HCA) receptors. Annu Rev Pharmacol Toxicol 54:407–434.  https://doi.org/10.1146/annurev-pharmtox-011613-135945 Google Scholar
  37. 37.
    Leurs R, Bakker RA, Timmerman H, de Esch IJ (2005) The histamine H3 receptor: from gene cloning to H3 receptor drugs. Nat Rev Drug Discov 4(2):107–120.  https://doi.org/10.1038/nrd1631 Google Scholar
  38. 38.
    Hansen AH, Sergeev E, Pandey SK, Hudson BD, Christiansen E, Milligan G, Ulven T (2017) Development and characterization of a fluorescent tracer for the free fatty acid receptor 2 (FFA2/GPR43). J Med Chem 60(13):5638–5645.  https://doi.org/10.1021/acs.jmedchem.7b00338 Google Scholar
  39. 39.
    Muredda L, Kepczynska MA, Zaibi MS, Alomar SY, Trayhurn P (2018) IL-1beta and TNFalpha inhibit GPR120 (FFAR4) and stimulate GPR84 (EX33) and GPR41 (FFAR3) fatty acid receptor expression in human adipocytes: implications for the anti-inflammatory action of n-3 fatty acids. Arch Physiol Biochem 124(2):97–108.  https://doi.org/10.1080/13813455.2017.1364774 Google Scholar
  40. 40.
    Tang C, Offermanns S (2017) FFA2 and FFA3 in metabolic regulation. Handb Exp Pharmacol 236:205–220.  https://doi.org/10.1007/164_2016_50 Google Scholar
  41. 41.
    Priyadarshini M, Wicksteed B, Schiltz GE, Gilchrist A, Layden BT (2016) SCFA receptors in pancreatic beta cells: novel diabetes targets? Trends Endocrinol Metab 27(9):653–664.  https://doi.org/10.1016/j.tem.2016.03.011 Google Scholar
  42. 42.
    Chambers ES, Morrison DJ, Frost G (2015) Control of appetite and energy intake by SCFA: what are the potential underlying mechanisms? Proc Nutr Soc 74(3):328–336.  https://doi.org/10.1017/s0029665114001657 Google Scholar
  43. 43.
    Cani PD, Neyrinck AM, Maton N, Delzenne NM (2005) Oligofructose promotes satiety in rats fed a high-fat diet: involvement of glucagon-like Peptide-1. Obes Res 13(6):1000–1007.  https://doi.org/10.1038/oby.2005.117 Google Scholar
  44. 44.
    Holmes E, Li JV, Marchesi JR, Nicholson JK (2012) Gut microbiota composition and activity in relation to host metabolic phenotype and disease risk. Cell Metab 16(5):559–564.  https://doi.org/10.1016/j.cmet.2012.10.007 Google Scholar
  45. 45.
    Chambers ES, Viardot A, Psichas A, Morrison DJ, Murphy KG, Zac-Varghese SE, MacDougall K, Preston T, Tedford C, Finlayson GS, Blundell JE, Bell JD, Thomas EL, Mt-Isa S, Ashby D, Gibson GR, Kolida S, Dhillo WS, Bloom SR, Morley W, Clegg S, Frost G (2015) Effects of targeted delivery of propionate to the human colon on appetite regulation, body weight maintenance and adiposity in overweight adults. Gut 64(11):1744–1754.  https://doi.org/10.1136/gutjnl-2014-307913 Google Scholar
  46. 46.
    Qin J, Li R, Raes J, Arumugam M, Burgdorf KS, Manichanh C, Nielsen T, Pons N, Levenez F, Yamada T, Mende DR, Li J, Xu J, Li S, Li D, Cao J, Wang B, Liang H, Zheng H, Xie Y, Tap J, Lepage P, Bertalan M, Batto JM, Hansen T, Le Paslier D, Linneberg A, Nielsen HB, Pelletier E, Renault P, Sicheritz-Ponten T, Turner K, Zhu H, Yu C, Li S, Jian M, Zhou Y, Li Y, Zhang X, Li S, Qin N, Yang H, Wang J, Brunak S, Dore J, Guarner F, Kristiansen K, Pedersen O, Parkhill J, Weissenbach J, Meta HITC, Bork P, Ehrlich SD, Wang J (2010) A human gut microbial gene catalogue established by metagenomic sequencing. Nature 464(7285):59–65.  https://doi.org/10.1038/nature08821 Google Scholar
  47. 47.
    Mondot S, de Wouters T, Dore J, Lepage P (2013) The human gut microbiome and its dysfunctions. Dig Dis 31(3–4):278–285.  https://doi.org/10.1159/000354678 Google Scholar
  48. 48.
    Xu J, Gordon JI (2003) Honor thy symbionts. Proc Natl Acad Sci U S A 100(18):10452–10459.  https://doi.org/10.1073/pnas.1734063100 Google Scholar
  49. 49.
    Devkota S, Wang Y, Musch MW, Leone V, Fehlner-Peach H, Nadimpalli A, Antonopoulos DA, Jabri B, Chang EB (2012) Dietary-fat-induced taurocholic acid promotes pathobiont expansion and colitis in Il10-/- mice. Nature 487(7405):104–108.  https://doi.org/10.1038/nature11225 Google Scholar
  50. 50.
    Lam V, Su J, Koprowski S, Hsu A, Tweddell JS, Rafiee P, Gross GJ, Salzman NH, Baker JE (2012) Intestinal microbiota determine severity of myocardial infarction in rats. FASEB J : official publication of the Federation of American Societies for Experimental Biology 26(4):1727–1735.  https://doi.org/10.1096/fj.11-197921 Google Scholar
  51. 51.
    Cani PD, Amar J, Iglesias MA, Poggi M, Knauf C, Bastelica D, Neyrinck AM, Fava F, Tuohy KM, Chabo C, Waget A, Delmee E, Cousin B, Sulpice T, Chamontin B, Ferrieres J, Tanti JF, Gibson GR, Casteilla L, Delzenne NM, Alessi MC, Burcelin R (2007) Metabolic endotoxemia initiates obesity and insulin resistance. Diabetes 56(7):1761–1772.  https://doi.org/10.2337/db06-1491 Google Scholar
  52. 52.
    Santos NCSAC, Castanho MA et al (2003) Evaluation of lipopolysaccharide aggregation by light scattering spectroscopy. Chembiochem 4(1):96–100Google Scholar
  53. 53.
    Furet JP, Kong LC, Tap J et al (2010) Differential adaptation of human gut microbiota to bariatric surgery-induced weight loss: links with metabolic and low-grade inflammation markers. Diabetes 59(12):3049–3057Google Scholar
  54. 54.
    Louis S, Tappu RM, Damms-Machado A, Huson DH, Bischoff SC (2016) Characterization of the gut microbial community of obese patients following a weight-loss intervention using whole metagenome shotgun sequencing. PLoS One 11(2):e0149564.  https://doi.org/10.1371/journal.pone.0149564 Google Scholar
  55. 55.
    Medzhitov R, Horng T (2009) Transcriptional control of the inflammatory response. Nat Rev Immunol 9(10):692–703.  https://doi.org/10.1038/nri2634 Google Scholar
  56. 56.
    Taira RYS, Shimizu K et al (2015) Bacterial cell wall components regulate adipokine secretion from visceral adipocytes. J Clin Biochem Nutr 56(2):149–154.  https://doi.org/10.3164/jcbn.14/74 Google Scholar
  57. 57.
    Everard A, Belzer C, Geurts L, Ouwerkerk JP, Druart C, Bindels LB, Guiot Y, Derrien M, Muccioli GG, Delzenne NM, de Vos WM, Cani PD (2013) Cross-talk between Akkermansia muciniphila and intestinal epithelium controls diet-induced obesity. Proc Natl Acad Sci U S A 110(22):9066–9071.  https://doi.org/10.1073/pnas.1219451110 Google Scholar
  58. 58.
    Laugerette F, Vors C, Geloen A, Chauvin MA, Soulage C, Lambert-Porcheron S, Peretti N, Alligier M, Burcelin R, Laville M, Vidal H, Michalski MC (2011) Emulsified lipids increase endotoxemia: possible role in early postprandial low-grade inflammation. J Nutr Biochem 22(1):53–59.  https://doi.org/10.1016/j.jnutbio.2009.11.011 Google Scholar
  59. 59.
    Blaut M (2015) Gut microbiota and energy balance: role in obesity. Proc Nutr Soc 74(3):227–234.  https://doi.org/10.1017/S0029665114001700 Google Scholar
  60. 60.
    Cani PD, Bibiloni R, Knauf C, Waget A, Neyrinck AM, Delzenne NM, Burcelin R (2008) Changes in gut microbiota control metabolic endotoxemia-induced inflammation in high-fat diet-induced obesity and diabetes in mice. Diabetes 57(6):1470–1481.  https://doi.org/10.2337/db07-1403 Google Scholar
  61. 61.
    Suzuki T (2013) Regulation of intestinal epithelial permeability by tight junctions. Cell Mol Life Sci : CMLS 70(4):631–659.  https://doi.org/10.1007/s00018-012-1070-x Google Scholar
  62. 62.
    Chaudhry KK, Samak G, Shukla PK, Mir H, Gangwar R, Manda B, Isse T, Kawamoto T, Salaspuro M, Kaihovaara P, Dietrich P, Dragatsis I, Nagy LE, Rao RK (2015) ALDH2 deficiency promotes ethanol-induced gut barrier dysfunction and fatty liver in mice. Alcohol Clin Exp Res 39(8):1465–1475.  https://doi.org/10.1111/acer.12777 Google Scholar
  63. 63.
    Vijay-Kumar M, Aitken JD, Carvalho FA, Cullender TC, Mwangi S, Srinivasan S, Sitaraman SV, Knight R, Ley RE, Gewirtz AT (2010) Metabolic syndrome and altered gut microbiota in mice lacking toll-like receptor 5. Science 328(5975):228–231.  https://doi.org/10.1126/science.1179721 Google Scholar
  64. 64.
    Rocha DM, Caldas AP, Oliveira LL, Bressan J, Hermsdorff HH (2016) Saturated fatty acids trigger TLR4-mediated inflammatory response. Atherosclerosis 244:211–215.  https://doi.org/10.1016/j.atherosclerosis.2015.11.015 Google Scholar
  65. 65.
    Fasano A (2011) Zonulin and its regulation of intestinal barrier function: the biological door to inflammation, autoimmunity, and cancer. Physiol Rev 91(1):151–175Google Scholar
  66. 66.
    Drucker DJ (2001) Glucagon-like peptide 2. J Clin Endocrinol Metab 86(4):1759Google Scholar
  67. 67.
    Delzenne NM, Neyrinck AM, Backhed F, Cani PD (2011) Targeting gut microbiota in obesity: effects of prebiotics and probiotics. Nat Rev Endocrinol 7(11):639–646.  https://doi.org/10.1038/nrendo.2011.126 Google Scholar
  68. 68.
    Cox AJ, West NP, Cripps AW (2015) Obesity, inflammation, and the gut microbiota. Lancet Diab Endocrinol 3(3):207–215.  https://doi.org/10.1016/s2213-8587(14)70134-2 Google Scholar
  69. 69.
    Creely S, Mc Ternan PG, Kusminski CM et al (2007) Lipopolysaccharide activates an innate immune system response in human adipose tissue in obesity and type 2 diabetes. Am J Physiol Endocrinol Metab 292(3):E740.  https://doi.org/10.1152/ajpendo.00302.2006.-Type Google Scholar
  70. 70.
    Pussinen PJ, Havulinna AS, Lehto M, Sundvall J, Salomaa V (2011) Endotoxemia is associated with an increased risk of incident diabetes. Diabetes Care 34(2):392–397.  https://doi.org/10.2337/dc10-1676 Google Scholar
  71. 71.
    Bibbo S, Ianiro G, Gasbarrini A, Cammarota G (2017) Fecal microbiota transplantation: past, present and future perspectives. Minerva Gastroenterol Dietol 63(4):420–430.  https://doi.org/10.23736/s1121-421x.17.02374-1 Google Scholar
  72. 72.
    Eiseman B, Silen W, Bascom GS, Kauvar AJ (1958) Fecal enema as an adjunct in the treatment of pseudomembranous enterocolitis. Surgery 44(5):854–859Google Scholar
  73. 73.
    Kassam Z, Lee CH, Yuan Y, Hunt RH (2013) Fecal microbiota transplantation for Clostridium difficile infection: systematic review and meta-analysis. Am J Gastroenterol 108(4):500–508.  https://doi.org/10.1038/ajg.2013.59 Google Scholar
  74. 74.
    Vrieze A, Van Nood E, Holleman F, Salojarvi J, Kootte RS, Bartelsman JF, Dallinga-Thie GM, Ackermans MT, Serlie MJ, Oozeer R, Derrien M, Druesne A, Van Hylckama Vlieg JE, Bloks VW, Groen AK, Heilig HG, Zoetendal EG, Stroes ES, de Vos WM, Hoekstra JB, Nieuwdorp M (2012) Transfer of intestinal microbiota from lean donors increases insulin sensitivity in individuals with metabolic syndrome. Gastroenterology 143(4):913–916 e917.  https://doi.org/10.1053/j.gastro.2012.06.031 Google Scholar
  75. 75.
    Zhang H, DiBaise JK, Zuccolo A, Kudrna D, Braidotti M, Yu Y, Parameswaran P, Crowell MD, Wing R, Rittmann BE, Krajmalnik-Brown R (2009) Human gut microbiota in obesity and after gastric bypass. Proc Natl Acad Sci U S A 106(7):2365–2370.  https://doi.org/10.1073/pnas.0812600106 Google Scholar
  76. 76.
    Duboc H, Nguyen CC, Cavin JB, Ribeiro-Parenti L, Jarry AC, Rainteau D, Humbert L, Coffin B, Le Gall M, Bado A, Sokol H (2018) Roux-en-Y Gastric-Bypass and sleeve gastrectomy induces specific shifts of the gut microbiota without altering the metabolism of bile acids in the intestinal lumen. Int J Obes 43(2):428–431 (2005) undefined (undefined):undefinedGoogle Scholar
  77. 77.
    Cani PD (2018) Severe obesity and gut microbiota: does bariatric surgery really reset the system? Gut 68(1):5–6. gutjnl-2018-316815.  https://doi.org/10.1136/gutjnl-2018-316815 Google Scholar
  78. 78.
    Trehan I, Goldbach HS, LaGrone LN, Meuli GJ, Wang RJ, Maleta KM, Manary MJ (2016) Antibiotics as part of the management of severe acute malnutrition. Malawi Med J : the journal of Medical Association of Malawi 28(3):123–130Google Scholar
  79. 79.
    Hernandez E, Bargiela R, Diez MS, Friedrichs A, Perez-Cobas AE, Gosalbes MJ, Knecht H, Martinez-Martinez M, Seifert J, von Bergen M, Artacho A, Ruiz A, Campoy C, Latorre A, Ott SJ, Moya A, Suarez A, Martins dos Santos VA, Ferrer M (2013) Functional consequences of microbial shifts in the human gastrointestinal tract linked to antibiotic treatment and obesity. Gut Microbes 4(4):306–315.  https://doi.org/10.4161/gmic.25321 Google Scholar
  80. 80.
    Nguyen SG, Kim J, Guevarra RB, Lee JH, Kim E, Kim SI, Unno T (2016) Laminarin favorably modulates gut microbiota in mice fed a high-fat diet. Food Funct 7(10):4193–4201.  https://doi.org/10.1039/c6fo00929h Google Scholar
  81. 81.
    Zheng J, Yuan X, Cheng G, Jiao S, Feng C, Zhao X, Yin H, Du Y, Liu H (2018) Chitosan oligosaccharides improve the disturbance in glucose metabolism and reverse the dysbiosis of gut microbiota in diabetic mice. Carbohydr Polym 190:77–86.  https://doi.org/10.1016/j.carbpol.2018.02.058 Google Scholar
  82. 82.
    Chang CJ, Lin CS, Lu CC, Martel J, Ko YF, Ojcius DM, Tseng SF, Wu TR, Chen YY, Young JD, Lai HC (2015) Ganoderma lucidum reduces obesity in mice by modulating the composition of the gut microbiota. Nat Commun 6:7489.  https://doi.org/10.1038/ncomms8489 Google Scholar
  83. 83.
    Delzenne NM, Bindels LB (2015) Gut microbiota: Ganoderma lucidum, a new prebiotic agent to treat obesity? Nat Rev Gastroenterol Hepatol 12(10):553–554.  https://doi.org/10.1038/nrgastro.2015.137 Google Scholar
  84. 84.
    Roopchand DE, Carmody RN, Kuhn P et al (2015) Dietary polyphenols promote growth of the gut bacterium Akkermansia muciniphila and attenuate high-fat diet-induced metabolic syndrome. Diabetes 64(8):2847–2858.  https://doi.org/10.2337/db14-1916/-/DC1 Google Scholar
  85. 85.
    Yoo JY, Kim SS (2016) Probiotics and prebiotics: present status and future perspectives on metabolic disorders. Nutrients 8(3):173.  https://doi.org/10.3390/nu8030173 Google Scholar
  86. 86.
    Anselmo AC, McHugh KJ, Webster J, Langer R, Jaklenec A (2016) Layer-by-layer encapsulation of probiotics for delivery to the microbiome. Adv Mater (Deerfield Beach, Fla) 28(43):9486–9490.  https://doi.org/10.1002/adma.201603270 Google Scholar
  87. 87.
    Moya-Perez A, Neef A, Sanz Y (2015) Bifidobacterium pseudocatenulatum CECT 7765 reduces obesity-associated inflammation by restoring the lymphocyte-macrophage balance and gut microbiota structure in high-fat diet-fed mice. PLoS One 10(7):e0126976.  https://doi.org/10.1371/journal.pone.0126976 Google Scholar
  88. 88.
    Fontane L, Benaiges D, Goday A, Llaurado G, Pedro-Botet J (2018) Influence of the microbiota and probiotics in obesity. Clinica e investigacion en arteriosclerosis : publicacion oficial de la Sociedad Espanola de Arteriosclerosis.  https://doi.org/10.1016/j.arteri.2018.03.004
  89. 89.
    Okubo T, Takemura N, Yoshida A, Sonoyama K (2013) KK/Ta mice administered Lactobacillus plantarum strain no. 14 have lower adiposity and higher insulin sensitivity. Biosci Microbiota Food Health 32(3):93–100.  https://doi.org/10.12938/bmfh.32.93 Google Scholar
  90. 90.
    Million M, Angelakis E, Paul M, Armougom F, Leibovici L, Raoult D (2012) Comparative meta-analysis of the effect of Lactobacillus species on weight gain in humans and animals. Microb Pathog 53(2):100–108.  https://doi.org/10.1016/j.micpath.2012.05.007 Google Scholar
  91. 91.
    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 Google Scholar
  92. 92.
    Mariat D, Firmesse O, Levenez F, Guimaraes V, Sokol H, Dore J, Corthier G, Furet JP (2009) The Firmicutes/Bacteroidetes ratio of the human microbiota changes with age. BMC Microbiol 9:123.  https://doi.org/10.1186/1471-2180-9-123 Google Scholar
  93. 93.
    Wu GD, Chen J, Hoffmann C, Bittinger K, Chen YY, Keilbaugh SA, Bewtra M, Knights D, Walters WA, Knight R, Sinha R, Gilroy E, Gupta K, Baldassano R, Nessel L, Li H, Bushman FD, Lewis JD (2011) Linking long-term dietary patterns with gut microbial enterotypes. Science 334(6052):105–108.  https://doi.org/10.1126/science.1208344 Google Scholar
  94. 94.
    Ley RE, Turnbaugh PJ, Klein S, Gordon JI (2006) Microbial ecology: human gut microbes associated with obesity. Nature 444(7122):1022–1023.  https://doi.org/10.1038/4441022a Google Scholar
  95. 95.
    Sonnenburg ED, Smits SA, Tikhonov M, Higginbottom SK, Wingreen NS, Sonnenburg JL (2016) Diet-induced extinctions in the gut microbiota compound over generations. Nature 529(7585):212–215.  https://doi.org/10.1038/nature16504 Google Scholar
  96. 96.
    Haghikia A, Jorg S, Duscha A, Berg J, Manzel A, Waschbisch A, Hammer A, Lee DH, May C, Wilck N, Balogh A, Ostermann AI, Schebb NH, Akkad DA, Grohme DA, Kleinewietfeld M, Kempa S, Thone J, Demir S, Muller DN, Gold R, Linker RA (2016) Dietary fatty acids directly impact central nervous system autoimmunity via the small intestine. Immunity 44(4):951–953.  https://doi.org/10.1016/j.immuni.2016.04.006 Google Scholar
  97. 97.
    Semova I, Carten JD, Stombaugh J, Mackey LC, Knight R, Farber SA, Rawls JF (2012) Microbiota regulate intestinal absorption and metabolism of fatty acids in the zebrafish. Cell Host Microbe 12(3):277–288.  https://doi.org/10.1016/j.chom.2012.08.003 Google Scholar
  98. 98.
    Gauffin Cano P, Santacruz A, Moya A, Sanz Y (2012) Bacteroides uniformis CECT 7771 ameliorates metabolic and immunological dysfunction in mice with high-fat-diet induced obesity. PLoS One 7(7):e41079.  https://doi.org/10.1371/journal.pone.0041079 Google Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Guangdong Engineering Research Center of Natural Products and New Drugs, Guangdong Provincial University Engineering Technology Research Center of Natural Products and DrugsGuangdong Pharmaceutical UniversityGuangzhouChina
  2. 2.Guangdong Metabolic Diseases Research Centre of Integrated Chinese and Western Medicine, Guangdong TCM Key Laboratory for Metabolic Diseases, Key Laboratory of Modulating Liver to Treat Hyperlipemia SATCM, Level 3 Laboratory of Lipid Metabolism SATCM, Institute of Chinese Medicinal SciencesGuangdong Pharmaceutical UniversityGuangzhouChina
  3. 3.School of Chemistry and Chemical EngineeringGuangdong Pharmaceutical UniversityZhongshanChina

Personalised recommendations