Skip to main content
SpringerLink
Log in

A Comprehensive Understanding of Dietary Effects on C. elegans Physiology

  • Published:
Current Medical Science Aims and scope Submit manuscript

Summary

Diet has been shown to play an important role in human physiology. It is a predominant exogenous factor regulating the composition of gut microbiota, and dietary intervention holds promise for treatment of diseases such as obesity, type 2 diabetes, and malnutrition. Furthermore, it was reported that diet has significant effects on physiological processes of C. elegans, including reproduction, fat storage, and aging. To reveal novel signaling pathways responsive to different diets, C. elegans and its bacterial diet were used as an interspecies model system to mimic the interaction between host and gut microbiota. Most signaling pathways identified in C. elegans are highly conserved across different species, including humans. A better understanding of these pathways can, therefore, help to develop interventions for human diseases. In this article, we summarize recent achievements on molecular mechanisms underlying the response of C. elegans to different diets and discuss their relevance to human health.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. Tilman D, Clark M. Global diets link environmental sustainability and human health. Nature, 2014, 515 (7528):518–522

    Article  CAS  PubMed  Google Scholar 

  2. Mcevoy CT, Temple N, Woodside JV. Vegetarian diets, low-meat diets and health: a review. Public Health Nutr, 2012,15(12):2287–2294

    Article  PubMed  Google Scholar 

  3. Bushman FD, Lewis JD, Wu GD. Diet, gut enterotypes and health: is there a link? Nestle Nutr Inst Workshop Ser, 2013,77:65–73

    Article  CAS  PubMed  Google Scholar 

  4. Xu Z, Knight R. Dietary effects on human gut microbiome diversity. Br J Nutr, 2015,113(Suppl):S1–S5

    Article  CAS  PubMed  Google Scholar 

  5. Smith P, Willemsen D, Popkes M, et al. Regulation of life span by the gut microbiota in the short-lived African turquoise killifish. Elife, 2017,6:e27014

    Article  PubMed  PubMed Central  Google Scholar 

  6. Jubair WK, Hendrickson JD, Severs EL, et al. Modulation of inflammatory arthritis by gut microbiota through mucosal inflammation and autoantibody generation. Arthritis Rheumatol, 2018,70(8):1220–1233

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Mulak A, Bonaz B. Brain-gut-microbiota axis in Parkinson’s disease. World J Gastroenterol, 2015,21(37):10609–10620

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Trompette A, Gollwitzer E S, Yadava K, et al. Gut microbiota metabolism of dietary fiber influences allergic airway disease and hematopoiesis. Nat Med, 2014,20(2):159–166

    Article  CAS  PubMed  Google Scholar 

  9. Wang X, Zhang L, Wang Y, et al. Gut microbiota dysbiosis is associated with Henoch-Schonlein Purpura in children. Int Immunopharmacol, 2018,58:1–8

    Article  CAS  PubMed  Google Scholar 

  10. Zhao L, Zhang F, Ding X, et al. Gut bacteria selectively promoted by dietary fibers alleviate type 2 diabetes. Science, 2018,359(6380):1151–1156

    Article  CAS  PubMed  Google Scholar 

  11. Koh A, De Vadder F, Kovatcheva-Datchary P, et al. From Dietary Fiber to Host Physiology: Short-Chain Fatty Acids as Key Bacterial Metabolites. Cell, 2016,165(6):1332–1345

    Article  CAS  PubMed  Google Scholar 

  12. Gopalakrishnan V, Spencer CN, Nezi L, et al. Gut microbiome modulates response to anti-PD-1 immunotherapy in melanoma patients. Science, 2018,359(6371):97–103

    Article  CAS  PubMed  Google Scholar 

  13. Matson V, Fessler J, Bao R, et al. The commensal microbiome is associated with anti-PD-1 efficacy in metastatic melanoma patients. Science, 2018,359(6371): 104–108

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Gibson MK, Crofts TS, Dantas G. Antibiotics and the developing infant gut microbiota and resistome. Curr Opin Microbiol, 2015,27:51–56

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Watson E, Macneil LT, Ritter AD, et al. Interspecies Systems Biology Uncovers Metabolites Affecting C. elegans Gene Expression and Life History Traits. Cell, 2014,156(6):1336–1337

    Article  CAS  PubMed  Google Scholar 

  16. Zhang J, Holdorf AD, Walhout AJ. C. elegans and its bacterial diet as a model for systems-level understanding of host-microbiota interactions. Curr Opin Biotechnol, 2017,46:74–80

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  17. Soukas AA, Kane EA, Carr CE, et al. Rictor/TORC2 regulates fat metabolism, feeding, growth, and life span in Caenorhabditis elegans. Genes Dev, 2009,23(4):496–511

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Gracida X, Eckmann C R. Fertility and germline stem cell maintenance under different diets requires nhr-114/HNF4 in C. elegans. Curr Biol, 2013,23(7):607–613

    Article  CAS  PubMed  Google Scholar 

  19. Brooks KK, Liang B, Watts JL. The influence of bacterial diet on fat storage in C. elegans. PLoS One, 2009,4(10):e7545

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  20. Han B, Sivaramakrishnan P, Lin CJ, et al. Microbial Genetic Composition Tunes Host Longevity. Cell, 2017,169(7):1249–1262

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Xiao R, Chun L, Ronan EA, et al. RNAi Interrogation of Dietary Modulation of Development, Metabolism, Behavior, and Aging in C. elegans. Cell Rep, 2015,11(7):1123–1133

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Gusarov I, Gautier L, Smolentseva O, et al. Bacterial nitric oxide extends the lifespan of C. elegans. Cell, 2013,152(4):818–830

    Article  CAS  PubMed  Google Scholar 

  23. Clark L C, Hodgkin J. Commensals, probiotics and pathogens in the Caenorhabditis elegans model. Cell Microbiol, 2014,16(1):27–38

    Article  CAS  PubMed  Google Scholar 

  24. Hoyles L, Jimenez-Pranteda ML, Chilloux J, et al. Metabolic retroconversion of trimethylamine N-oxide and the gut microbiota. Microbiome, 2018,6(1):73

    Article  PubMed  PubMed Central  Google Scholar 

  25. Scott TA, Quintaneiro LM, Norvaisas P, et al. Host-Microbe Co-metabolism Dictates Cancer Drug Efficacy in C. elegans. Cell, 2017,169(3):442–456

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. García-González AP, Ritter AD, Shrestha S. Bacterial Metabolism Affects the C. elegans Response to Cancer Chemotherapeutics. Cell, 2017,169(3):431–441

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  27. Offer SM, Diasio RB. Is It Finally Time for a Personalized Medicine Approach for Fluorouracil-Based Therapies? J Clin Oncol, 2016,34(3):205–207

    Article  CAS  PubMed  Google Scholar 

  28. Iida N, Dzutsev A, Stewart CA, et al. Commensal bacteria control cancer response to therapy by modulating the tumor microenvironment. Science, 2013,342(6161): 967–970

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Harris G, Shen Y, Ha H, et al. Dissecting the signaling mechanisms underlying recognition and preference of food odors. J Neurosci, 2014,34(28):9389–9403

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  30. Song BM, Faumont S, Lockery S, et al. Recognition of familiar food activates feeding via an endocrine serotonin signal in Caenorhabditis elegans. Elife, 2013,2:e329

    Google Scholar 

  31. Gray JM, Hill JJ, Bargmann CI. A circuit for navigation in Caenorhabditis elegans. Proc Natl Acad Sci USA, 2005,102(9):3184–3191

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Apfeld J, Kenyon C. Regulation of lifespan by sensory perception in Caenorhabditis elegans. Nature, 1999,402(6763):804–809

    Article  CAS  PubMed  Google Scholar 

  33. Maier W, Adilov B, Regenass M, et al. A neuromedin U receptor acts with the sensory system to modulate food type-dependent effects on C. elegans lifespan. PLoS Biol, 2010,8(5):e1000376

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  34. Spanier B, Lasch K, Marsch S, et al. How the intestinal peptide transporter PEPT-1 contributes to an obesity phenotype in Caenorhabditits elegans. PLoS One, 2009,4(7):e6279

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  35. Nehrke K. A reduction in intestinal cell pHi due to loss of the Caenorhabditis elegans Na+/H+ exchanger NHX-2 increases life span. J Biol Chem, 2003,278(45):44657–44666

    Article  CAS  PubMed  Google Scholar 

  36. Takano A, Usui I, Haruta T, et al. Mammalian target of rapamycin pathway regulates insulin signaling via subcellular redistribution of insulin receptor substrate 1 and integrates nutritional signals and metabolic signals of insulin. Mol Cell Biol, 2001,21(15):5050–5062

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Tremblay F, Marette A. Amino acid and insulin signaling via the mTOR/p70 S6 kinase pathway. A negative feedback mechanism leading to insulin resistance in skeletal muscle cells. J Biol Chem, 2001,276(41):38052–38060

    Article  CAS  PubMed  Google Scholar 

  38. Haruta T, Uno T, Kawahara J, et al. A rapamycin-sensitive pathway down-regulates insulin signaling via phosphorylation and proteasomal degradation of insulin receptor substrate-1. Mol Endocrinol, 2000,14(6):783–794

    Article  CAS  PubMed  Google Scholar 

  39. Edinger AL, Thompson CB. Akt maintains cell size and survival by increasing mTOR-dependent nutrient uptake. Mol Biol Cell, 2002,13(7):2276–2288

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Long X, Ortiz-Vega S, Lin Y, et al. Rheb binding to mammalian target of rapamycin (mTOR) is regulated by amino acid sufficiency. J Biol Chem, 2005,280(25):23433–23436

    Article  CAS  PubMed  Google Scholar 

  41. Mizunuma M, Neumann-Haefelin E, Moroz N, et al. mTORC2-SGK-1 acts in two environmentally responsive pathways with opposing effects on longevity. Aging Cell, 2014,13(5):869–878

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Gao AW, Chatzispyrou IA, Kamble R, et al. A sensitive mass spectrometry platform identifies metabolic changes of life history traits in C. elegans. Sci Rep, 2017,7(1):2408

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  43. Reinke SN, Hu X, Sykes BD, et al. Caenorhabditis elegans diet significantly affects metabolic profile, mitochondrial DNA levels, lifespan and brood size. Mol Genet Metab, 2010,100(3):274–282

    Article  CAS  PubMed  Google Scholar 

  44. Rooks MG, Garrett WS. Gut microbiota, metabolites and host immunity. Nat Rev Immunol, 2016,16(6):341–352

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Pang S, Curran SP. Adaptive capacity to bacterial diet modulates aging in C. elegans. Cell Metab, 2014,19(2): 221–231

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Banerjee R, Ragsdale S W. The many faces of vitamin B12: catalysis by cobalamin-dependent enzymes. Annu Rev Biochem, 2003,72:209–247

    Article  CAS  PubMed  Google Scholar 

  47. Amanda Jacobson LLMR. A Gut Commensal-Produced Metabolite Mediates Colonization Resistance to Salmonella Infection. Cell Host Microbe, 2018,24(2):296–307

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  48. Wei CC, Yen PL, Chang ST, et al. Antioxidative Activities of Both Oleic Acid and Camellia tenuifolia Seed Oil Are Regulated by the ranscription Factor DAF-16/FOXO in Caenorhabditis elegans. PLoS One, 2016,11(6):e157195

    Google Scholar 

  49. Wu K, Gao X, Shi B, et al. Enriched endogenous n-3 polyunsaturated fatty acids alleviate cognitive and behavioral deficits in a mice model of Alzheimer’s disease. Neuroscience, 2016,333:345–355

    Article  CAS  PubMed  Google Scholar 

  50. Han S, Schroeder EA, Silva-Garcia CG, et al. Monounsaturated fatty acids link H3K4me3 modifiers to C. elegans lifespan. Nature, 2017,544(7649):185–190

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Sugawara S, Honma T, Ito J, et al. Fish oil changes the lifespan of Caenorhabditis elegans via lipid peroxidation. J Clin Biochem Nutr, 2013,52(2):139–145

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. O’Rourke EJ, Kuballa P, Xavier R, et al. omega-6 Polyunsaturated fatty acids extend life span through the activation of autophagy. Genes Dev, 2013,27(4):429–440

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  53. Lynn DA, Dalton HM, Sowa JN, et al. Omega-3 and -6 fatty acids allocate somatic and germline lipids to ensure fitness during nutrient and oxidative stress in Caenorhabditis elegans. Proc Natl Acad Sci USA, 2015,112(50):15378–15383

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Ma DK, Li Z, Lu AY, et al. Acyl-CoA Dehydrogenase Drives Heat Adaptation by Sequestering Fatty Acids. Cell, 2015,161(5):1152–1163

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Kahn-Kirby AH, Dantzker JL, Apicella AJ, et al. Specific polyunsaturated fatty acids drive TRPV-dependent sensory signaling in vivo. Cell, 2004,119(6):889–900

    Article  CAS  PubMed  Google Scholar 

  56. Du D, Shi YH, Le GW. Microarray analysis of high-glucose diet-induced changes in mRNA expression in jejunums of C57BL/6J mice reveals impairment in digestion, absorption. Mol Biol Rep, 2010,37(4):1867–1874

    Article  CAS  PubMed  Google Scholar 

  57. Carsten LD, Watts T, Markow TA. Gene expression patterns accompanying a dietary shift in Drosophila melanogaster. Mol Ecol, 2005,14(10):3203–3208

    Article  CAS  PubMed  Google Scholar 

  58. Murfin KE, Whooley AC, Klassen JL, et al. Comparison of Xenorhabdus bovienii bacterial strain genomes reveals diversity in symbiotic functions. BMC Genomics, 2015,16:889

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  59. Dunbar TL, Yan Z, Balla KM, et al. C. elegans detects pathogen-induced translational inhibition to activate immune signaling. Cell Host Microbe, 2012,11(4):375–386

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Macneil LT, Watson E, Arda HE, et al. Diet-induced developmental acceleration independent of TOR and insulin in C. elegans. Cell, 2013,153(1):240–252

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

We thank Bi ZHANG, Guang LI, Xu LIU, and other members of Professor Liu’s laboratory for their assistance in this manuscript.

Author information

Authors and Affiliations

  1. Collaborative Innovation Center for Brain Science, College of Life Science and Technology, Huazhong University of Science and Technology, Wuhan, 430074, China

    Jie-jun Zhou, Lei Chun & Jian-feng Liu

Authors
  1. Jie-jun Zhou
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Lei Chun
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jian-feng Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Lei Chun or Jian-feng Liu.

Additional information

Conflict of Interest Statement

The authors declare that there is no conflict of interest relevant to this article.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zhou, Jj., Chun, L. & Liu, Jf. A Comprehensive Understanding of Dietary Effects on C. elegans Physiology. CURR MED SCI 39, 679–684 (2019). https://doi.org/10.1007/s11596-019-2091-6

Download citation

  • Received:

  • Revised:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11596-019-2091-6

Key words

Search

Navigation