Microbial transcriptional responses to host diet maintain gut microbiome homeostasis in the American cockroach

Diet is considered a key determinant of gut microbiome composition and function. However, studies in the American cockroach have revealed surprising stability in hindgut microbiome taxonomic composition following shifts in host diet. To discover microbial activities underlying this stability, we analyzed microbial community transcriptomes from hindguts of cockroaches fed diverse diets. We used a taxon-centric approach in which we clustered genomes based on taxonomic relatedness and functional similarity and examined the transcriptional profiles of each cluster independently. In total, we analyzed a set of 18 such "genome clusters", including key taxa within Bacteroidota, Bacillota, Desulfobacterota, and Euryarcheaeota phyla. We found that microbial transcriptional responses to diet varied across diets and microbial functional profiles, with the strongest transcriptional shifts seen in taxa predicted to be primarily focused on degradation of complex dietary polysaccharides. These groups upregulated genes associated with utilization of diet-sourced polysaccharides in response to bran and dog food diets, while they upregulated genes for degradation of potentially host-derived polysaccharides in response to tuna, butter, and starvation diets. In contrast, chemolithotrophic taxa, such as Desulfobacterota and Methanimicrococcus, exhibited stable transcriptional profiles, suggesting that compensatory changes in the metabolism of other microbial community members are sufficient to support their activities across major dietary shifts. These results provide new insight into microbial activities supporting gut microbiome stability in the face of variable diets in omnivores.