Core-predominant gut fungus Kazachstania slooffiae promotes intestinal epithelial glycolysis via lysine desuccinylation in pigs

Abstract

Background Gut fungi are increasingly recognized as important contributors to host physiology, although most studies have focused on gut bacteria. Post-translational modifications (PTMs) of proteins play vital roles in cell metabolism. However, the contribution of gut fungi to host protein PTMs remains unclear. Mining gut fungi that mediate host protein PTMs and dissecting their mechanism are urgently needed. Results We studied the gut fungal communities of 56 weaned piglets and 56 finishing pigs from seven pig breeds using internal transcribed spacer (ITS) gene amplicon sequencing and metagenomics. The results showed that Kazachstania slooffiae was the most abundant gut fungal species in the seven breeds of weaned piglets. K. slooffiae decreased intestinal epithelial lysine succinylation levels, and these proteins were especially enriched in the glycolysis pathway. We demonstrated that K. slooffiae promoted intestinal epithelial glycolysis by decreasing lysine succinylation by activating sirtuin 5 (SIRT5). Furthermore, K. slooffiae-derived 5′-methylthioadenosine metabolite promoted the SIRT5 activity. Conclusions These findings provide a landscape of gut fungal communities of pigs and suggest that K. slooffiae plays a crucial role in intestinal glycolysis metabolism through lysine desuccinylation. Our data also suggest a potential protective strategy for pigs with an insufficient intestinal energy supply.

Weaning transition, but not the administration of probiotic candidate Kazachstania slooffiae, shaped the gastrointestinal bacterial and fungal communities in nursery piglets

“…As piglets are already stressed during the weaning transition and administration takes time and handling, orally gavaging piglets daily is not practical. Additionally, the previous studies ( 18 , 42 ) both reported higher CFU in their dosages and more frequent administration than those used here. Here, if sample collection and treatment overlapped on the same day, samples were collected from pigs before treatment.…”

“…In this study, feeding K. slooffiae to piglets before and during the weaning transition was studied to determine impacts on health and growth performance. K. slooffiae has been consistently observed as a commensal in the pig gastrointestinal tract and has shown positive interactions with beneficial commensal bacteria in vitro ( 13–16 , 22 , 42 ); thus, we hypothesized that feeding K. slooffiae as a probiotic would improve piglet performance through: (a) indirect modulation of the combined microbiome ( 13 ); or (b) direct effects due to increased abundance of K. slooffiae in the gastrointestinal tract ( 18 , 19 ). Overall, we did not observe any improvements in piglet health or growth as an effect of K. slooffiae treatment, nor any detectable, sustained differences on alpha and beta diversity within either the bacteriome or mycobiome at day 49 as a direct result of supplementation.…”

“…Finally, a number of cytokines were compared for animals at day 14 (before any treatments were administered) and day 49 (4 weeks after the last treatment given) from serum samples to determine if administration of K. slooffiae could have an effect aside from improving the metabolism of cells within the intestinal lining ( 42 ), such as improved immune function from a systemic level. For almost all cytokines where there was a treatment by age interaction, there were no differences between treatments at day 49, indicating K. slooffiae administration likely does not have any long-term effects on systemic immunological response in piglets.…”

Effects of lactic acid bacteria isolated from Tibetan chickens on the growth performance and gut microbiota of broiler

“…Evidence shows that this sort of alternation of gut microbiota (often called dysbiosis) cause all sorts of health issues including diarrhea and inflammation ( Cerf-Bensussan and Gaboriau-Routhiau, 2010 ; Nagalingam et al, 2011 ; Arfken et al, 2020 ; Rutkowski et al, 2022 ; Uthaibutra et al, 2023 ). Overall, the balance of the intestinal microbiota is critical for maintaining the health of intestine and regulating the growth of the animal ( He et al, 2022 ; Hu et al, 2023 ).…”

Massive expansion of the pig gut virome based on global metagenomic mining

“…The gut microbiota is a complex microbial ecosystem that plays crucial roles in pig health, nutrient metabolism, and productivity (Chen et al, 2021a;Hu et al, 2023;Wang et al, 2022;Yang et al, 2022). Pig intestinal virus infections are prevalent in the global pig industry, but the large numbers of diverse viruses that inhabit the pig gut can greatly affect the structure and function of the gut microbial ecosystem (Shkoporov et al, 2022a).…”