Spilling their guts: Digestive symbionts of turtle ants can overcome host’s dietary challenges

Bacterial symbionts can support animal nutrition by facilitating digestion of plant dietary fibers. The symbiosis between turtle ants (genus Cephalotes) and their gut bacteria provides an ideal model to study the nature and evolution of insect-bacteria nutritional symbioses. Cephalotes adult workers host abundant and diverse gut bacteria, that are conserved across Cephalotes species. While these adult-associated symbionts recycle nitrogen, I hypothesize that they also aid the digestion of their host’s pollen-rich diet. Additionally, nothing is known about the roles of the environmentally-acquired bacterial symbionts of larvae. To explore bacterial contributions toward Cephalotes-host nutrition, we used shotgun metagenomics and metatranscriptomics on Cephalotes guts. Among larval gut bacteria, environmentally-acquired Enterobacteriales can catabolize abundant dietary fibers including cellulose, hemicelluloses, lignins, starches and two types of pectins – homogalacturonan, rhamnogalacturonan-I. The specialized, coevolved bacterial symbionts of Cephalotes adults similarly encode a range of fiber-catabolizing enzymes, degrading cellulose, hemicelluloses, lignins, starches and rhamnogalacturonan-I. Our metatranscriptomic analyses reveal that this microbiome dynamically responds to changes in C. varians worker diets, with specialized symbionts from the bacterial orders Pseudomonadales, Sphingobacteriales and Xanthomonadales expressing genes for the degradation of cellulose, hemicelluloses and rhamnogalacturonan-I on pollen-rich, versus control, diets. This diverse arsenal of symbiotic digestive enzymes among Cephalotes life stages suggests conserved, symbiont-enhanced degradation of several dietary fibers in both larvae and adults. Spanning Cephalotes hosts with up to 45 million years of divergence, these symbiont-conferred digestive capacities provide a plausible suite of key dietary adaptations, with potentially large influence on the ecological success of this diverse ant group.