Niche specialization and cross-feeding interactions shaping gut microbial fiber degradation in a model omnivore

The gut microbiome plays an active role in host health, producing gut metabolites that influence host digestive and immune function while also mediating microbial crosstalk. Dietary fiber is a major source of important fermentation byproducts that are generally implicated in gut community stability and host wellbeing, but dissecting microbe-specific contributions to polysaccharide metabolism in the context of a complex gut community is challenging with conventional model organisms. Using the American cockroach (Periplaneta americana) as a model omnivore, we use chemically-defined synthetic diets to identify how complex gut microbial communities respond to two of the most abundant plant polysaccharides, xylan and cellulose. To do so, we fed cockroaches synthetic diets containing one of these fibers or a mix of both in differing ratios. Through both 16S rRNA gene profiling and RNA-seq, we show that mixed fibers enrich for organisms characteristic of the source fibers as well as additional organisms only enriched in mixed-fiber diets. Through an organism-centric pangenome approach, we identify the impact of these fibers on gut microbiome activity. We found that gut communities responded strongly to xylan, with Bacteroidota belonging to Bacteroides, Dysgonomonas, and Parabacteroides producing xylan-active CAZymes at high levels. Multiple groups of Bacillota also responded strongly to a xylan diet, but appeared to act as cross-feeding secondary degraders, producing primarily xylosidases and transcripts associated with xylose utilization. In contrast, cellulose diets were associated with higher transcriptional activity among Fibrobacterota, which are typically a minor component of the cockroach gut microbiome but were the primary producers of CAZymes associated with cellulose and cellobiose degradation. These experiments provide new insight into gut microbial metabolism of these complex plant polysaccharides. Further, they highlight the utility of the cockroach model and synthetic diets to answer fundamental questions about gut microbial responses to different polysaccharides alone and in combination.