Division mechanism of labor in Diqing Tibetan Pigs gut microbiota for dietary fiber efficiently utilization

Abstract

Abstract Background The Diqing Tibetan (DT) pig is an herbivorous breed that inhabits an area with the highest altitude distribution in the world and can be maintained on a diet containing 90% forage material in confinement production systems. The possible association between specialized gut microorganisms and the efficient utilization of dietary fiber in this breed are unclear. Results Digestibility analysis showed that DT pigs had a strong capability for high-efficiency utilization of arabinose and xylose. Microorganisms in the cecum preferred to use xylan and uronic acid, while colonic microorganisms were better at using cellulose, glucan and mannan. Metagenomic analysis revealed that the high expression of feruloyl esterase, endo-β-1,4-xylanase, β-1,3-D-glucosidase, β-mannosidase, β-1,3(4)-glucanase and reducing-end xylanase in the intestinal microorganisms of these pigs was a decisive factor for the efficient utilization of nonstarch polysaccharides. The secretion of carbohydrate esterases was mainly undertaken by fecal strains of Microbacterium, Alistipes, Acinetobacter, and Faecalibacterium, while Microbacterium, Prevotella, Turicibacter, Lactobacillus, Clostridium and Streptococcus were responsible for most of the secretion of glycoside hydrolases. Then, a new species of Microbacterium was captured and appeared to have the highest fiber utilization ability in vitro, degrading 36.54% of the neutral detergent fiber in corn stover. The results of whole genome sequencing showed that the 16S rRNA sequence similarity between the strain and the microorganisms in the database was less than 97.113%, and the average nucleotide identity (ANI) was less than 95%. The strain was finally determined to be a brand new species, which was named Microbacterium sp. Qiao 01. Then, a total of 161 carbohydrate enzyme genes were annotated, including 80 glycoside hydrolases, 40 glycosyltransferases, 26 carbohydrate esterases, 11 auxiliary oxidoreductase, 3 polysaccharide lyases and 1 carbohydrate domain. Conclusions Our results provide strong evidence that efficient utilization of dietary fiber by DT pigs is due to the emergence of highly specialized microbial strategies in the gut. Microorganisms showed preferences and a clear division of labor in the degradation process of dietary fiber. Microbacterium sp. Qiao 01 was the key player in the efficient utilization of nonstarch polysaccharides in DT pigs. This study may inspire novel approaches for the deep excavation of high-quality microbial resources in regional species and has great practical significance for improving the utilization efficiency of livestock feed and alleviating the tension of food insecurity.