Exploration of symbiont metabolic potentials in the Antillean turtle ant (Cephalotes varians) gut

Gut bacterial symbionts can support animal nutrition by facilitating digestion and providing valuable metabolites. While the composition of gut symbiont communities shifts with host development in holometabolous insects, changes in symbiotic roles are not well documented, especially in ants. Here, we explored the metabolic capabilities of microbiomes sampled from herbivorous turtle ant (Cephalotes varians) larvae and adult workers. We used comprehensive genomic and metagenomic screenings and in vitro targeted metabolic assays to investigate bacterial functions at symbiont and gut community levels. We reveal that larval guts harbor environmentally-acquired bacterial symbionts in abundance, but share two Rhizobiales symbiont species with their adult nestmates. These larval gut bacteria encode impressive metabolic capabilities, including degradation and fermentation of plant and fungal cell wall components obtained from the host-ant diet. Surprisingly, several members of the adult gut symbionts, sampled downstream of an anatomic barrier that dams large food particles, have conserved their abilities to depolymerize complex dietary fibers. This adult symbiont digestion may be enabled by anal-oral transfers of gut symbionts among adult nestmates. Additionally, symbionts from both life stages can recycle nitrogen, synthesize organic acids, and B vitamins, and metabolize sulfur. With the help of their gut symbionts, turtle ant larvae can be seen as an important component of the turtle ant colony nutrition. Yet, thanks to their conserved gut symbionts, adult workers appear well-equipped to face their dietary challenges even in a larval-independent fashion.