Review Article

Fungal Alterations in Inflammatory Bowel Diseases

Siu Lam; Tao Zuo; Martin Ho; Francis K. L. Chan; Paul K. S. Chan; Siew C. Ng

Disclosures

Aliment Pharmacol Ther. 2019;50(11):1159-1171. 

In This Article

Influence of Diet on Gut Fungi Composition and Abundance

Increasing evidence from animal, clinical, and epidemiological studies suggests that diet high in carbohydrates or animal fat, and low in fibre, is associated with an increased risk of IBD in genetically susceptible individuals. Modifying diets may reduce the risk of disease development or flare.[74] Diet has been shown to affect the fungal microbiota. In healthy individuals, a plant-based diet was associated with an increase in gut colonisation by Candida species, whereas the intake of an animal-based diet facilitated the expansion of Penicillium species.[75] Carbohydrates are a robust energy source for fungi and serve as a sugar component for cell wall remodelling and act as a tryptophan precursor when starved.[29,76–78] Studies showed that Candida species degraded complex carbohydrates and starch via fermentation to provide simpler sugars as an energy source to different types of microbes.[79,80]

Amino acids and proteins can impact the abundance of C albicans differently in in vivo and in vitro models.[29,81] In an in vivo model, Hoffmann et al reported a negative association between the abundance of C albicans and amino acid uptake.[29] In contrast, an in vitro model by Miramón and Lorenz showed that C albicans were positively associated with amino acid consumption because the fungus converts amino acids into carbohydrates. The newly formed carbohydrates were used to neutralise the acidic environment of the phagolysosome, thereby subverting macrophages' cytotoxicity.[81] These two distinct results suggest that amino acids serve as a nutrient source for C albicans; fungi with higher possession of amino acids are more likely to survive in the gut, provided these fungi can convert amino acids into carbohydrates and favour a relatively alkaline environment.[29,81] Competition for amino acid has been reported for C albicans and Lactobacillus, a Gram-positive bacterial population that was found to be suppressed in patients with IBD.[76,82,83] High consumption of dietary protein by the host led to the breakdown of tryptophan forming indoles via indoleamine 2,3-dioxygenase 1 (IDO1) secreted by Lactobacillus in the gut.[76,83] Aryl hydrocarbon receptor from the host was activated by the newly formed indoles. The activated Aryl hydrocarbon receptor further up-regulated Interleukin 22 (IL-22) and T-helper cell 17 to inhibit C albicans colonisation (Figure 1).[76,83]

Figure 1.

Association between host diet consumption and microbial metabolism. Complex sugar, carbohydrate and starch consumption provides energy source for the gut microbiota. Candida albicans degrades complex carbohydrates via fermentation, which provides simpler sugar as an energy source for inter-species Prevotella and Ruminococcus. Alternatively, carbohydrate is utilised by C albicans for cell wall remodelling and maintenance. On the other hand, fatty acid consumed by the host provides high saturated fat to the bacterial genus Lactobacillus. Fatty acids also increase taurine-conjugation to bile acid in the host liver, which is further reduced by accepting electrons from electron transport chain (ETC) to form an end-product hydrogen sulphide, supplying organic sulphur to the bacterial community. Other dietary components such as proteins are broken down to tryptophan, and they are taken by Lactobacillus. Lactobacillus breaks down tryptophan into indoles via indoleamine 2,3-dioxygenase 1 (IDO1). Indoles bind and activate the aryl hydrocarbon receptor (AhR) that up-regulates interleukin 22 (IL-22) and down-regulates T helper 17 cells (Th17) cells in opposing C albicans colonisation

Dietary fatty acids have been shown to affect the abundance of C albicans. For instance, high consumption of saturated fat increases taurine's conjugation to bile acid in the live, which forms hydrogen sulphide.[84,85] Hydrogen sulphide is the major source of organic sulphur that promotes Lactobacillus growth in the gut,[84–86] and exerts an inhibitory effect on C albicans leading to a reduced abundance (Figure 1).[84–86] Besides, short chain fatty acids can directly inhibit C albicans.[87] Conjugated linoleic acid was also reported to block C albicans transformation from yeast to the hypha form.[87] Conjugated linoleic acid impedes GTP-binding protein Ras1p's anchorage onto the intracellular membrane, and also suppresses mRNA and protein levels of GTPase RAS1, a key component of C albicans' cell cycle for hyphal transformation.[87]

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