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RESEARCH ARTICLE (Open Access)

Munching microbes: diet–microbiome interactions shape gut health and cancer outcomes

Emma Todd A , Reem Elnour A * , Rebecca Simpson B * , Miguel Castaneda C * and Erin R Shanahan A D
+ Author Affiliations
- Author Affiliations

A School of Life and Environmental Sciences, Charles Perkins Centre, University of Sydney, Camperdown, NSW, Australia

B Melanoma Institute Australia, Charles Perkins Centre, University of Sydney, Camperdown, NSW, Australia

C School of Medical Sciences, Charles Perkins Centre, University of Sydney, Camperdown, NSW, Australia

D Tel.: +61 2 8627 7113; Email: erin.shanahan@sydney.edu.au

Microbiology Australia 42(2) 60-64 https://doi.org/10.1071/MA21026
Submitted: 30 March 2021  Accepted: 20 May 2021   Published: 17 June 2021

Journal Compilation © The Authors 2021 Open Access CC BY-NC-ND, published (by CSIRO Publishing) on behalf of the ASM

Abstract

The gut microbiome describes the complex community of microorganisms that populate the gastrointestinal tract. Gut microbes in the large bowel utilise both dietary-derived nutrients, such as host-indigestible carbohydrates (fibre) and excess protein, host-derived nutrients (intestinal mucin), and also interact with the by-products of digestion such as bile acids. They transform these compounds into a series of metabolites that can profoundly shape host physiology both locally and systemically. These metabolites can fundamentally alter host outcomes, promoting either gut health, or sub-optimal conditions in the gut that contribute to poor health, including increased risk of cancer. The microbiome of an individual has also been shown to impact response to cancer treatment strategies, including both treatment efficacy and side-effects in the gut and more systemically. This makes the microbiome a powerful potential tool for therapeutic purposes, once we overcome the challenges associated with individual variation in microbial community composition. As the gut microbial ecosystem is primarily altered by nutrient availability, diet therefore represents an important asset in therapeutically altering the gut microbiome.


References

[1]  Statovci, D. et al. (2017) The impact of Western diet and nutrients on the microbiota and immune response at mucosal interfaces. Front. Immunol. 8, 838.
The impact of Western diet and nutrients on the microbiota and immune response at mucosal interfaces.Crossref | GoogleScholarGoogle Scholar | 28804483PubMed |

[2]  Tayyem, R.F. et al. (2015) Macro- and micronutrients consumption and the risk for colorectal cancer among Jordanians. Nutrients 7, 1769–1786.
Macro- and micronutrients consumption and the risk for colorectal cancer among Jordanians.Crossref | GoogleScholarGoogle Scholar | 25763533PubMed |

[3]  Chun, Y.J. et al. (2015) Associations of colorectal cancer incidence with nutrient and food group intakes in Korean adults: a case-control study. Clin. Nutr. Res. 4, 110–123.
Associations of colorectal cancer incidence with nutrient and food group intakes in Korean adults: a case-control study.Crossref | GoogleScholarGoogle Scholar | 25954732PubMed |

[4]  Liu, L. et al. (2011) Is dietary fat associated with the risk of colorectal cancer? A meta-analysis of 13 prospective cohort studies. Eur. J. Nutr. 50, 173–184.
Is dietary fat associated with the risk of colorectal cancer? A meta-analysis of 13 prospective cohort studies.Crossref | GoogleScholarGoogle Scholar | 20697723PubMed |

[5]  Sonnenburg, J.L. and Backhed, F. (2016) Diet-microbiota interactions as moderators of human metabolism. Nature 535, 56–64.
Diet-microbiota interactions as moderators of human metabolism.Crossref | GoogleScholarGoogle Scholar | 27383980PubMed |

[6]  Gibson, P.R. and Shepherd, S.J. (2005) Personal view: food for thought--western lifestyle and susceptibility to Crohn’s disease. The FODMAP hypothesis. Aliment. Pharmacol. Ther. 21, 1399–1409.
Personal view: food for thought--western lifestyle and susceptibility to Crohn’s disease. The FODMAP hypothesis.Crossref | GoogleScholarGoogle Scholar | 15948806PubMed |

[7]  Marsh, A. et al. (2016) Does a diet low in FODMAPs reduce symptoms associated with functional gastrointestinal disorders? A comprehensive systematic review and meta-analysis. Eur. J. Nutr. 55, 897–906.
Does a diet low in FODMAPs reduce symptoms associated with functional gastrointestinal disorders? A comprehensive systematic review and meta-analysis.Crossref | GoogleScholarGoogle Scholar | 25982757PubMed |

[8]  Koropatkin, N.M. et al. (2012) How glycan metabolism shapes the human gut microbiota. Nat. Rev. Microbiol. 10, 323–335.
How glycan metabolism shapes the human gut microbiota.Crossref | GoogleScholarGoogle Scholar | 22491358PubMed |

[9]  Reese, A.T. et al. (2018) Microbial nitrogen limitation in the mammalian large intestine. Nat. Microbiol. 3, 1441–1450.
Microbial nitrogen limitation in the mammalian large intestine.Crossref | GoogleScholarGoogle Scholar | 30374168PubMed |

[10]  Holmes, A.J. et al. (2017) Diet–microbiome interactions in health are controlled by intestinal nitrogen source constraints. Cell Metab. 25, 140–151.
Diet–microbiome interactions in health are controlled by intestinal nitrogen source constraints.Crossref | GoogleScholarGoogle Scholar | 27889387PubMed |

[11]  Hamilton, M.K. et al. (2015) Changes in intestinal barrier function and gut microbiota in high-fat diet-fed rats are dynamic and region dependent. Am. J. Physiol. Gastrointest. Liver Physiol. 308, G840–G851.
Changes in intestinal barrier function and gut microbiota in high-fat diet-fed rats are dynamic and region dependent.Crossref | GoogleScholarGoogle Scholar | 25747351PubMed |

[12]  Odenwald, M.A. and Turner, J.R. (2017) The intestinal epithelial barrier: a therapeutic target? Nat. Rev. Gastroenterol. Hepatol. 14, 9–21.
The intestinal epithelial barrier: a therapeutic target?Crossref | GoogleScholarGoogle Scholar | 27848962PubMed |

[13]  Tailford, L.E. et al. (2015) Mucin glycan foraging in the human gut microbiome. Front. Genet. 6, 81.
Mucin glycan foraging in the human gut microbiome.Crossref | GoogleScholarGoogle Scholar | 25852737PubMed |

[14]  Singh, N. et al. (2014) Activation of Gpr109a, receptor for niacin and the commensal metabolite butyrate, suppresses colonic inflammation and carcinogenesis. Immunity 40, 128–139.
Activation of Gpr109a, receptor for niacin and the commensal metabolite butyrate, suppresses colonic inflammation and carcinogenesis.Crossref | GoogleScholarGoogle Scholar | 24412617PubMed |

[15]  Macia, L. et al. (2015) Metabolite-sensing receptors GPR43 and GPR109A facilitate dietary fibre-induced gut homeostasis through regulation of the inflammasome. Nat. Commun. 6, 6734.
Metabolite-sensing receptors GPR43 and GPR109A facilitate dietary fibre-induced gut homeostasis through regulation of the inflammasome.Crossref | GoogleScholarGoogle Scholar | 25828455PubMed |

[16]  Canani, R.B. et al. (2011) Potential beneficial effects of butyrate in intestinal and extraintestinal diseases. World J. Gastroenterol. 17, 1519–1528.
Potential beneficial effects of butyrate in intestinal and extraintestinal diseases.Crossref | GoogleScholarGoogle Scholar | 21472114PubMed |

[17]  Wang, K. et al. (2019) Claudin-7 downregulation induces metastasis and invasion in colorectal cancer via the promotion of epithelial-mesenchymal transition. Biochem. Biophys. Res. Commun. 508, 797–804.
Claudin-7 downregulation induces metastasis and invasion in colorectal cancer via the promotion of epithelial-mesenchymal transition.Crossref | GoogleScholarGoogle Scholar | 30528239PubMed |

[18]  Furusawa, Y. et al. (2013) Commensal microbe-derived butyrate induces the differentiation of colonic regulatory T cells. Nature 504, 446–450.
Commensal microbe-derived butyrate induces the differentiation of colonic regulatory T cells.Crossref | GoogleScholarGoogle Scholar | 24226770PubMed |

[19]  Smith, P.M. et al. (2013) The microbial metabolites, short-chain fatty acids, regulate colonic Treg cell homeostasis. Science 341, 569–573.
The microbial metabolites, short-chain fatty acids, regulate colonic Treg cell homeostasis.Crossref | GoogleScholarGoogle Scholar | 23828891PubMed |

[20]  Desai, M.S. et al. (2016) A dietary fiber-deprived gut microbiota degrades the colonic mucus barrier and enhances pathogen susceptibility. Cell 167, 1339–1353.e21.
A dietary fiber-deprived gut microbiota degrades the colonic mucus barrier and enhances pathogen susceptibility.Crossref | GoogleScholarGoogle Scholar | 27863247PubMed |

[21]  O’Keefe, S.J.D. (2016) Diet, microorganisms and their metabolites and colon cancer. Nat. Rev. Gastroenterol. Hepatol. 13, 691–706.
Diet, microorganisms and their metabolites and colon cancer.Crossref | GoogleScholarGoogle Scholar |

[22]  Ridlon, J.M. et al. (2016) Consequences of bile salt biotransformations by intestinal bacteria. Gut Microbes 7, 22–39.
Consequences of bile salt biotransformations by intestinal bacteria.Crossref | GoogleScholarGoogle Scholar | 26939849PubMed |

[23]  Hang, S. et al. (2019) Bile acid metabolites control TH17 and Treg cell differentiation. Nature 576, 143–148.
Bile acid metabolites control TH17 and Treg cell differentiation.Crossref | GoogleScholarGoogle Scholar | 31776512PubMed |

[24]  Campbell, C. et al. (2020) Bacterial metabolism of bile acids promotes generation of peripheral regulatory T cells. Nature 581, 475–479.
Bacterial metabolism of bile acids promotes generation of peripheral regulatory T cells.Crossref | GoogleScholarGoogle Scholar | 32461639PubMed |

[25]  Biagioli, M. et al. (2017) The bile acid receptor GPBAR1 regulates the M1/M2 phenotype of intestinal macrophages and activation of GPBAR1 rescues mice from murine colitis. J. Immunol. 199, 718–733.
The bile acid receptor GPBAR1 regulates the M1/M2 phenotype of intestinal macrophages and activation of GPBAR1 rescues mice from murine colitis.Crossref | GoogleScholarGoogle Scholar | 28607110PubMed |

[26]  Bernstein, H. et al. (2005) Bile acids as carcinogens in human gastrointestinal cancers. Mutat. Res. Rev. Mutat. Res. 589, 47–65.
Bile acids as carcinogens in human gastrointestinal cancers.Crossref | GoogleScholarGoogle Scholar |

[27]  Cao, H. et al. (2014) The secondary bile acid, deoxycholate accelerates intestinal adenoma–adenocarcinoma sequence in Apc min/+ mice through enhancing Wnt signaling. 13, 563–571.
| 25106466PubMed |

[28]  O’Keefe, S.J.D. et al. (2015) Fat, fibre and cancer risk in African Americans and rural Africans. 6, 6342.

[29]  Gagnière, J. et al. (2016) Gut microbiota imbalance and colorectal cancer. World J. Gastroenterol. 22, 501–518.
Gut microbiota imbalance and colorectal cancer.Crossref | GoogleScholarGoogle Scholar | 26811603PubMed |

[30]  Kaiko, G.E. et al. (2016) The colonic crypt protects stem cells from microbiota-derived metabolites. Cell 165, 1708–1720.
The colonic crypt protects stem cells from microbiota-derived metabolites.Crossref | GoogleScholarGoogle Scholar | 27264604PubMed |

[31]  Gopalakrishnan, V. et al. (2018) Gut microbiome modulates response to anti-PD-1 immunotherapy in melanoma patients. Science 359, 97–103.
Gut microbiome modulates response to anti-PD-1 immunotherapy in melanoma patients.Crossref | GoogleScholarGoogle Scholar | 29097493PubMed |

[32]  Matson, V. et al. (2018) The commensal microbiome is associated with anti-PD-1 efficacy in metastatic melanoma patients. Science 359, 104–108.
The commensal microbiome is associated with anti-PD-1 efficacy in metastatic melanoma patients.Crossref | GoogleScholarGoogle Scholar | 29302014PubMed |

[33]  Routy, B. et al. (2018) Gut microbiome influences efficacy of PD-1-based immunotherapy against epithelial tumors. Science 359, 91–97.
Gut microbiome influences efficacy of PD-1-based immunotherapy against epithelial tumors.Crossref | GoogleScholarGoogle Scholar | 29097494PubMed |

[34]  Spencer, C.N. et al. (2019) Abstract 2838: The gut microbiome (GM) and immunotherapy response are influenced by host lifestyle factors. Cancer Res. 79, 2838.

[35]  Simpson, R.C. et al. (2021) Targeting the microbiome to overcome resistance. Cancer Cell 39, 151–153.
Targeting the microbiome to overcome resistance.Crossref | GoogleScholarGoogle Scholar | 33561397PubMed |

[36]  Batten, M. et al. (2020) Gut microbiota predicts response and toxicity with neoadjuvant immunotherapy. Cancer Res. 80, 5734.

[37]  Kovatcheva-Datchary, P. et al. (2015) Dietary fiber-induced improvement in glucose metabolism is associated with increased abundance of Prevotella. Cell Metab. 22, 971–982.
Dietary fiber-induced improvement in glucose metabolism is associated with increased abundance of Prevotella.Crossref | GoogleScholarGoogle Scholar | 26552345PubMed |

[38]  Healey, G. et al. (2016) Influence of habitual dietary fibre intake on the responsiveness of the gut microbiota to a prebiotic: protocol for a randomised, double-blind, placebo-controlled, cross-over, single-centre study. BMJ Open 6, e012504.
Influence of habitual dietary fibre intake on the responsiveness of the gut microbiota to a prebiotic: protocol for a randomised, double-blind, placebo-controlled, cross-over, single-centre study.Crossref | GoogleScholarGoogle Scholar | 27591024PubMed |

[39]  Patnode, M.L. et al. (2019) Interspecies competition impacts targeted manipulation of human gut bacteria by fiber-derived glycans. Cell 179, 59–73 e13.
Interspecies competition impacts targeted manipulation of human gut bacteria by fiber-derived glycans.Crossref | GoogleScholarGoogle Scholar | 31539500PubMed |

[40]  Walker, A.W. et al. (2011) Dominant and diet-responsive groups of bacteria within the human colonic microbiota. ISME J. 5, 220–230.
Dominant and diet-responsive groups of bacteria within the human colonic microbiota.Crossref | GoogleScholarGoogle Scholar | 20686513PubMed |

[41]  Baxter, N.T. et al. (2019) Dynamics of human gut microbiota and short-chain fatty acids in response to dietary interventions with three fermentable fibers. MBio 10, e02566-18.
Dynamics of human gut microbiota and short-chain fatty acids in response to dietary interventions with three fermentable fibers.Crossref | GoogleScholarGoogle Scholar | 30696735PubMed |