Advertisement

Current Microbiology

, Volume 76, Issue 2, pp 237–247 | Cite as

Assessing the Influence of Dietary History on Gut Microbiota

  • Bo Yang
  • Chang Ye
  • Bingyu Yan
  • Xionglei He
  • Ke XingEmail author
Article

Abstract

Diet is known to play a major role in determining the composition and function of the gut microbiota. Previous studies have often focused on the immediate effects of dietary intervention. How dietary history prior to a given dietary intervention influences the gut microbiota is, however, not well understood. To assess the influence of dietary history, in this study, mice with different dietary histories were subjected to the same dietary interventions, and the gut microbial communities of these mice were characterized by 16S rDNA sequencing. We found that dietary history played a long-lasting role in the composition of the gut microbiota when the dietary switch was moderate. In sharp contrast, such effects nearly vanished when the diet was switched to certain extreme dietary conditions. Interestingly, the abundance of Akkermansia, a bacterial genus associated with loss of body weight, was elevated dramatically in mice subjected to a diet composed exclusively of meat. Our results revealed a more complex picture of the influence of dietary history on gut microbiota than anticipated.

Notes

Acknowledgements

We are grateful to members of the He lab for their discussion and comments on this manuscript. This work is supported by the Natural Science Foundation of Guangdong Province, China (Project No. 2017A030313121).

Compliance with Ethical Standards

Conflict of interest

The authors declare no conflict of interest.

Supplementary material

284_2018_1616_MOESM1_ESM.pdf (850 kb)
Supplementary material 1 (PDF 850 KB)

References

  1. 1.
    Allison SD, Martiny JB (2008) Colloquium paper: resistance, resilience, and redundancy in microbial communities. Proc Natl Acad Sci USA 105(Suppl 1):11512–11519.  https://doi.org/10.1073/pnas.0801925105 CrossRefPubMedGoogle Scholar
  2. 2.
    Arumugam M, Raes J et al (2011) Enterotypes of the human gut microbiome. Nature 473(7346):174–180.  https://doi.org/10.1038/nature09944 CrossRefPubMedPubMedCentralGoogle Scholar
  3. 3.
    Belzer C, de Vos WM (2012) Microbes inside from diversity to function: the case of Akkermansia. ISME J 6(8):1449–1458.  https://doi.org/10.1038/ismej.2012.6 CrossRefPubMedPubMedCentralGoogle Scholar
  4. 4.
    Bergström A, Skov TH et al (2014) Establishment of intestinal microbiota during early life: a longitudinal, explorative study of a large cohort of Danish infants. Appl Environ Microbiol 80(9):2889–2900.  https://doi.org/10.1128/AEM.00342-14 CrossRefPubMedPubMedCentralGoogle Scholar
  5. 5.
    Bernier JF, Calvert CC, Famula TR, Baldwin RL (1986) Maintenance energy requirement and net energetic efficiency in mice with a major gene for rapid postweaning gain. J Nutr 116(3):419–428.  https://doi.org/10.1093/jn/116.3.419 CrossRefPubMedGoogle Scholar
  6. 6.
    Biasucci G, Benenati B, Morelli L, Bessi E, Boehm G (2008) Cesarean delivery may affect the early biodiversity of intestinal bacteria. J Nutr 138(9):1796S–1800SCrossRefPubMedGoogle Scholar
  7. 7.
    Cabrera-Rubio R, Collado MC et al (2012) The human milk microbiome changes over lactation and is shaped by maternal weight and mode of delivery. Am J Clin Nutr 96(3):544–551.  https://doi.org/10.3945/ajcn.112.037382 CrossRefPubMedGoogle Scholar
  8. 8.
    Caporaso JG, Lauber CL et al (2011) Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample. Proc Natl Acad Sci USA 108(Suppl 1):4516–4522.  https://doi.org/10.1073/pnas.1000080107 CrossRefPubMedGoogle Scholar
  9. 9.
    Carmody RN, Gerber GK et al (2015) Diet dominates host genotype in shaping the murine gut microbiota. Cell Host Microbe 17(1):72–84.  https://doi.org/10.1016/j.chom.2014.11.010 CrossRefGoogle Scholar
  10. 10.
    Chen J, Bittinger K et al (2012) Associating microbiome composition with environmental covariates using generalized UniFrac distances. Bioinformatics 28(16):2106–2113.  https://doi.org/10.1093/bioinformatics/bts342 CrossRefPubMedPubMedCentralGoogle Scholar
  11. 11.
    Claesson MJ, Jeffery IB et al (2012) Gut microbiota composition correlates with diet and health in the elderly. Nature 488(7410):178–184.  https://doi.org/10.1038/nature11319 CrossRefGoogle Scholar
  12. 12.
    Chu DM, Antony KM et al (2016) The early infant gut microbiome varies in association with a maternal high-fat diet. Genome Med 8(1):77.  https://doi.org/10.1186/s13073-016-0330-z CrossRefPubMedPubMedCentralGoogle Scholar
  13. 13.
    Collins KH, Paul HA et al (2016) A high-fat high-sucrose diet rapidly alters muscle integrity, inflammation and gut microbiota in male rats. Sci Rep 6:37278.  https://doi.org/10.1038/srep37278 CrossRefPubMedPubMedCentralGoogle Scholar
  14. 14.
    Dao MC, Everard A et al (2016) Akkermansia muciniphila and improved metabolic health during a dietary intervention in obesity: relationship with gut microbiome richness and ecology. Gut 65(3):426–436.  https://doi.org/10.1136/gutjnl-2014-308778 CrossRefGoogle Scholar
  15. 15.
    David LA, Maurice CF et al (2014) Diet rapidly and reproducibly alters the human gut microbiome. Nature 505(7484):559–563.  https://doi.org/10.1038/nature12820 CrossRefPubMedPubMedCentralGoogle Scholar
  16. 16.
    De Filippo C, Cavalieri D et al (2010) Impact of diet in shaping gut microbiota revealed by a comparative study in children from Europe and rural Africa. Proc Natl Acad Sci USA 107(33):14691–14696.  https://doi.org/10.1073/pnas.1005963107 CrossRefPubMedGoogle Scholar
  17. 17.
    Derrien M, Belzer C, de Vos WM (2017) Akkermansia muciniphila and its role in regulating host functions. Microb Pathog 106:171–181.  https://doi.org/10.1016/j.micpath.2016.02.005 CrossRefGoogle Scholar
  18. 18.
    Derrien M, Collado MC, Ben-Amor K, Salminen S, de Vos WM (2008) The Mucin degrader Akkermansia muciniphila is an abundant resident of the human intestinal tract. Appl Environ Microbiol 74(5):1646–1648.  https://doi.org/10.1128/AEM.01226-07 CrossRefGoogle Scholar
  19. 19.
    Derrien M, Vaughan EE, Plugge CM, de Vos WM (2004) Akkermansia muciniphila gen. nov., sp. nov., a human intestinal mucin-degrading bacterium. Int J Syst Evol Microbiol 54(Pt 5):1469–1476.  https://doi.org/10.1099/ijs.0.02873-0 CrossRefGoogle Scholar
  20. 20.
    DeSantis TZ, Hugenholtz P et al (2006) Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Applied Environ Microbiol 72(7):5069–5072.  https://doi.org/10.1128/AEM.03006-05 CrossRefGoogle Scholar
  21. 21.
    Dominguez-Bello MG, Costello EK et al (2010) Delivery mode shapes the acquisition and structure of the initial microbiota across multiple body habitats in newborns. Proc Natl Acad Sci USA 107(26):11971–11975.  https://doi.org/10.1073/pnas.1002601107 CrossRefGoogle Scholar
  22. 22.
    Edgar RC (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26(19):2460–2461.  https://doi.org/10.1093/bioinformatics/btq461 CrossRefGoogle Scholar
  23. 23.
    Everard A, Belzer C et al (2013) Cross-talk between Akkermansia muciniphila and intestinal epithelium controls diet-induced obesity. Proc Natl Acad Sci USA 110(22):9066–9071.  https://doi.org/10.1073/pnas.1219451110 CrossRefGoogle Scholar
  24. 24.
    Everard A, Lazarevic V et al (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 CrossRefPubMedPubMedCentralGoogle Scholar
  25. 25.
    Faith JJ, Guruge JL et al (2013) The long-term stability of the human gut microbiota. Science 341(6141):1237439.  https://doi.org/10.1126/science.1237439 CrossRefPubMedPubMedCentralGoogle Scholar
  26. 26.
    Faith JJ, McNulty NP, Rey FE, Gordon JI (2011) Predicting a human gut microbiota’s response to diet in gnotobiotic mice. Science 333(6038):101–104.  https://doi.org/10.1126/science.1206025 CrossRefPubMedPubMedCentralGoogle Scholar
  27. 27.
    Gill SR, Pop M et al (2006) Metagenomic analysis of the human distal gut microbiome. Science 312(5778):1355–1359.  https://doi.org/10.1126/science.1124234 CrossRefPubMedPubMedCentralGoogle Scholar
  28. 28.
    Girardot C, Scholtalbers J, Sauer S, Su SY, Furlong EE (2016) Je, a versatile suite to handle multiplexed NGS libraries with unique molecular identifiers. BMC Bioinformatics 17(1):419.  https://doi.org/10.1186/s12859-016-1284-2 CrossRefPubMedPubMedCentralGoogle Scholar
  29. 29.
    Guo J, Hall KD (2011) Predicting changes of body weight, body fat, energy expenditure and metabolic fuel selection in C57BL/6 mice. PLoS ONE 5(1):e15961.  https://doi.org/10.1371/journal.pone.0015961 6) .CrossRefGoogle Scholar
  30. 30.
    Hooper LV, Gordon JI (2001) Commensal host-bacterial relationships in the gut. Science 292(5519):1115–1118CrossRefGoogle Scholar
  31. 31.
    Human Microbiome Project C (2012) Structure, function and diversity of the healthy human microbiome. Nature 486(7402):207–214.  https://doi.org/10.1038/nature11234 CrossRefGoogle Scholar
  32. 32.
    Karlsson CL, Onnerfalt J et al (2012) The microbiota of the gut in preschool children with normal and excessive body weight. Obesity 20(11):2257–2261.  https://doi.org/10.1038/oby.2012.110 CrossRefPubMedGoogle Scholar
  33. 33.
    Koenig JE, Spor A et al (2011) Succession of microbial consortia in the developing infant gut microbiome. Proc Natl Acad Sci USA 108(Suppl 1):4578–4585.  https://doi.org/10.1073/pnas.1000081107 CrossRefGoogle Scholar
  34. 34.
    Lim MY, Rho M et al (2014) Stability of gut enterotypes in Korean monozygotic twins and their association with biomarkers and diet. Sci Rep 4:7348.  https://doi.org/10.1038/srep07348 CrossRefPubMedPubMedCentralGoogle Scholar
  35. 35.
    Lozupone CA, Stombaugh JI, Gordon JI, Jansson JK, Knight R (2012) Diversity, stability and resilience of the human gut microbiota. Nature 489(7415):220–230.  https://doi.org/10.1038/nature11550 CrossRefPubMedPubMedCentralGoogle Scholar
  36. 36.
    Ma J, Prince AL et al (2014) High-fat maternal diet during pregnancy persistently alters the offspring microbiome in a primate model. Nat Commun 5:3889.  https://doi.org/10.1038/ncomms4889 CrossRefPubMedPubMedCentralGoogle Scholar
  37. 37.
    McMurdie PJ1, Holmes S (2013) phyloseq: an R package for reproducible interactive analysis and graphics of microbiome census data. PLoS ONE 8(4):e61217.  https://doi.org/10.1371/journal.pone.0061217 CrossRefPubMedPubMedCentralGoogle Scholar
  38. 38.
    Muegge BD, Kuczynski J et al (2011) Diet drives convergence in gut microbiome functions across mammalian phylogeny and within humans. Science 332(6032):970–974.  https://doi.org/10.1126/science.1198719 CrossRefPubMedPubMedCentralGoogle Scholar
  39. 39.
    Paul HA, Bomhof MR, Vogel HJ, Reimer RA (2016) Diet-induced changes in maternal gut microbiota and metabolomic profiles influence programming of offspring obesity risk in rats. Sci Rep 6:20683.  https://doi.org/10.1038/srep20683 CrossRefPubMedPubMedCentralGoogle Scholar
  40. 40.
    Rajilic-Stojanovic M, Heilig HG, Tims S, Zoetendal EG, de Vos WM (2012) Long-term monitoring of the human intestinal microbiota composition. Environ Microbiol.  https://doi.org/10.1111/1462-2920.12023 CrossRefPubMedGoogle Scholar
  41. 41.
    Rutayisire E, Huang K, Liu Y, Tao F (2016) The mode of delivery affects the diversity and colonization pattern of the gut microbiota during the first year of infants’ life: a systematic review. BMC Gastroenterol 16(1):86.  https://doi.org/10.1186/s12876-016-0498-0 CrossRefPubMedPubMedCentralGoogle Scholar
  42. 42.
    Schneeberger M, Everard A et al (2015) Akkermansia muciniphila inversely correlates with the onset of inflammation, altered adipose tissue metabolism and metabolic disorders during obesity in mice. Sci Rep 5:16643.  https://doi.org/10.1038/srep16643 CrossRefPubMedPubMedCentralGoogle Scholar
  43. 43.
    Shin NR, Lee JC et al (2014) An increase in the Akkermansia spp. population induced by metformin treatment improves glucose homeostasis in diet-induced obese mice. Gut 63(5):727–735.  https://doi.org/10.1136/gutjnl-2012-303839 CrossRefGoogle Scholar
  44. 44.
    Sonnenburg ED, Smits SA et al (2016) Diet-induced extinctions in the gut microbiota compound over generations. Nature 529(7585):212–215.  https://doi.org/10.1038/nature16504 CrossRefPubMedPubMedCentralGoogle Scholar
  45. 45.
    Swiatecka D, Narbad A, Ridgway KP, Kostyra H (2011) The study on the impact of glycated pea proteins on human intestinal bacteria. Int J Food Microbiol 145(1):267–272.  https://doi.org/10.1016/j.ijfoodmicro.2011.01.002 CrossRefGoogle Scholar
  46. 46.
    Turnbaugh PJ, Hamady M et al (2009) A core gut microbiome in obese and lean twins. Nature 457(7228):480–484.  https://doi.org/10.1038/nature07540 CrossRefGoogle Scholar
  47. 47.
    Turnbaugh PJ, Ley RE et al (2006) An obesity-associated gut microbiome with increased capacity for energy harvest. Nature 444(7122):1027–1031.  https://doi.org/10.1038/nature05414 CrossRefGoogle Scholar
  48. 48.
    Wang Q, Garrity GM, Tiedje JM, Cole JR (2007) Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol 73(16):5261–5267.  https://doi.org/10.1128/AEM.00062-07 CrossRefPubMedPubMedCentralGoogle Scholar
  49. 49.
    Wang Y, Xu L, Liu J, Zhu W, Mao S (2017) A high grain diet dynamically shifted the composition of mucosa-associated microbiota and induced mucosal injuries in the colon of sheep. Front Microbiol.  https://doi.org/10.3389/fmicb.2017.02080 CrossRefPubMedPubMedCentralGoogle Scholar
  50. 50.
    Wu GD, Chen J et al (2011) Linking long-term dietary patterns with gut microbial enterotypes. Science 334(6052):105–108.  https://doi.org/10.1126/science.1208344 CrossRefPubMedPubMedCentralGoogle Scholar
  51. 51.
    Zhang C, Zhang M et al (2012) Structural resilience of the gut microbiota in adult mice under high-fat dietary perturbations. ISME J 6(10):1848–1857.  https://doi.org/10.1038/ismej.2012.27 CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  1. 1.State Key Laboratory of Biocontrol, School of Life SciencesSun Yat-sen UniversityGuangzhouChina
  2. 2.Affiliated Cancer Hospital & Institute of Guangzhou Medical UniversityGuangzhouChina
  3. 3.School of Life SciencesGuangzhou UniversityGuangzhouChina

Personalised recommendations