Interactions between gut microbes and host promote degradation of various fiber components in Meishan pigs.

Abstract

Although metagenomic investigations into microbial fiber-degrading capabilities are currently prevalent, there is a notable gap in research concerning the regulatory mechanisms underpinning host-microbiota interactions that confer tolerance to high-fiber diets in pigs. In this study, 28 Meishan (MS) and 28 Large White (LW) pigs were subjected to feeding experiments involving various fiber levels. Subsequently, multi-omics was employed to investigate the influence of host-microbiota interactions on the fiber degradation of pigs. MS exhibited superior fiber digestibility compared with LW, particularly evident when fed a high-fiber diet. In MS, positive interactions among Treponema bryantii, Treponema sp., Rikenellaceae bacterium, and Bacteroidales bacterium WCE2004 facilitated the degradation of both cellulose and pectin. The reduced polymerization of polysaccharides and oligosaccharides observed in MS provides compelling evidence for their superior microbial fiber-degrading capability. The concentrations of propionate and butyrate retained in cecal lumen of MS was unchanged, whereas it was significantly increased in LW, indicating a strong absorption of short-chain fatty acids (SCFAs) in MS intestines. Correlation analysis using RNA-seq data revealed distinct patterns in LW and MS. In LW, microbial profiles along with GPR183 and GPR174 exhibited negative correlations with butyrate and propionate, respectively. Conversely, in MS, GPR174 and SLC2A4 were positively correlated with butyrate. Our findings underscore the dynamic collaboration among microbial species in degrading cellulose and pectin, coupled with the synergistic effects of SCFA transport-related genes, as crucial underpinnings for the heightened fiber digestibility observed in MS. These discoveries offer fresh perspectives into the intricate mechanisms governing host-microbiota interactions that influence fiber digestion in pigs.

Importance: Studies on porcine intestinal microbiota have been widely conducted, and some microbial taxa with fiber degradation functions have been identified. However, the mechanisms of division among gut microbes in the degradation of complex fiber components are still unclear. In addition, the regulation of fiber digestion by host through absorption of short-chain fatty acids (SCFAs) needs to be further investigated. Our study used apparent total tract digestibility of dietary fiber to assess the utilization efficiency of dietary fiber between Meishan and Large White pigs. Subsequently, through metagenome sequencing and determination of fiber-degrading products, we found that in Meishan pigs, positive interactions among Treponema bryantii, Treponema sp., Rikenellaceae bacterium, and Bacteroidales bacterium WCE2004 facilitated the degradation of both cellulose and pectin. RNA-seq analysis elucidated breed-specific genes associated with SCFA absorption in cecum. By integrating multi-omics data, we constructed a framework outlining host-microbiota interactions that control dietary fiber utilization in pigs. Our data provide novel insights into host-microbiota interactions regulating fiber degradation and lay some theoretical foundations for improving the utilization efficiency of high-fiber cereal feed in pigs through targeted modulation of gut microbial function.