The Nutritional Significance of Intestinal Fungi: Alteration of Dietary Carbohydrate Composition Triggers Colonic Fungal Community Shifts in a Pig Model

Although fungi are a large group of microorganisms along with bacteria and archaea in the gut of monogastric animals, the nutritional significance of fungi has been ignored for a long time. Our previous studies revealed a distinct fungal community in the gut of grazing Tibetan pigs (1) and a close correlation between fungal species and short-chain fatty acids, the main microbial metabolites of carbohydrates in the hindgut of pigs (2). ABSTRACT Carbohydrates represent the most important energy source in the diet of humans and animals. A large number of studies have shown that dietary carbohydrates (DCHO) are related to the bacterial community in the gut, but their relationship with the composition of intestinal fungi is still unknown. Here, we report the response of the colonic fungal community to different compositions of DCHO in a pig model. Three factors, ratio (2:1, 1:1, and 1:2) of amylose to amylopectin (AM/AP), level of nonstarch polysaccharides (NSP; 1%, 2%, and 3%), and mannan-oligosaccharide (MOS; 400, 800, and 1,200 mg/kg body weight), were considered according to an L9 (34) orthogonal design to form nine diets with different carbohydrate compositions. Sequencing based on an Illumina HiSeq 2500 platform targeting the internal transcribed spacer 1 region showed that the fungal community in the colon of the pigs responded to DCHO in the order of MOS, AM/AP, and NSP. A large part of some low-abundance fungal genera correlated with the composition of DCHO, represented by Saccharomycopsis, Mrakia, Wallemia, Cantharellus, Eurotium, Solicoccozyma, and Penicillium, were also associated with the concentration of glucose and fructose, as well as the activity of β-d-glucosidase in the colonic digesta, suggesting a role of these fungi in the degradation of DCHO in the colon of pigs. Our study provides direct evidence for the relationship between the composition of DCHO and the fungal community in the colon of pigs, which is helpful to understand the function of gut microorganisms in pigs. IMPORTANCE Although fungi are a large group of microorganisms along with bacteria and archaea in the gut of monogastric animals, the nutritional significance of fungi has been ignored for a long time. Our previous studies revealed a distinct fungal community in the gut of grazing Tibetan pigs (J. Li, D. Chen, B. Yu, J. He, et al., Microb Biotechnol 13:509–521, 2020, https://doi.org/10.1111/1751-7915.13507) and a close correlation between fungal species and short-chain fatty acids, the main microbial metabolites of carbohydrates in the hindgut of pigs (J. Li, Y. Luo, D. Chen, B. Yu, et al., J Anim Physiol Anim Nutr 104:616–628, 2020, https://doi.org/10.1111/jpn.13300). These groundbreaking findings indicate a potential relationship between intestinal fungi and the utilization of DCHO. However, no evidence directly proves the response of intestinal fungi to changes in DCHO. Here, we show a clear alteration of the colonic fungal community in pigs triggered by different compositions of DCHO simulated by varied concentrations of starch, nonstarch polysaccharides (NSP), and oligosaccharides. Our results highlight the potential involvement of intestinal fungi in the utilization of nutrients in monogastric animals.