Nitrogen conservation, conserved: 46 million years of N-recycling by the core symbionts of turtle ants

Abstract

Nitrogen acquisition is a major challenge for herbivorous animals, and the repeated origins of herbivory across the ants have raised expectations that nutritional symbionts have shaped their diversification. Direct evidence for N-provisioning by internally housed symbionts is rare in animals; among the ants, it has been documented for just one lineage. In this study we dissect functional contributions by bacteria from a conserved, multi-partite gut symbiosis in herbivorous Cephalotes ants through in vivo experiments, (meta)genomics, and in vitro assays. Gut bacteria recycle urea, and likely uric acid, using recycled N to synthesize essential amino acids that are acquired by hosts in substantial quantities. Specialized core symbionts of 17 studied Cephalotes species encode the pathways directing these activities, and several recycle N in vitro. These findings point to a highly efficient N-economy, and a nutritional mutualism preserved for millions of years through the derived behaviors and gut anatomy of Cephalotes ants.CategoryBiological Sciences-Evolution

Localization of Bacterial Communities within Gut Compartments acrossCephalotesTurtle Ants

“…Urea, major component of mammal urine, is often ingested by Cephalotes species (22,23). The abundance of Cephaloticoccus found in the midgut, coupled with the discovery of urease-encoding capacities across this group suggests that they assist in urea metabolism (12).…”

“…These bacteria also encode glutamate dehydrogenase (gdhA) and have complete pathways for synthesizing most essential amino acids (12,86). This indicates that within the midgut Cephaloticoccus may have the capacity to convert urea into ammonia, ammonia into glutamate, and to subsequently use glutamate as an N-donor in synthesizing several essential amino acids (Fig.…”

“…For example, microbial symbionts have been hypothesized to largely enable the ant's ecological dominance throughout nutrient-limited rainforest canopies (7,8). In addition, broad molecular surveys have illustrated that symbiotic bacteria are correlated with the evolution of herbivory across ant species (9), while both experimentation and genomics have illustrated that herbivorous ants benefit from specialized, nitrogen recycling gut bacteria (10)(11)(12)(13)).…”

“…The ileum contains a combination of both partially digested liquid food and nitrogenous waste. The uric acid in the ileum likely derives from two sources: ingested bird excrement and output from the Malpighian tubules(12,32). Malpighian tubules spread into the Cephalotes body cavity and absorb nitrogenous waste, like uric acid, functioning as the main excretory organ of insects(3).…”

The scent of symbiosis: gut bacteria affect social interactions in leafcutting ants

“…Gut bacteria play essential metabolic roles in several ant species, such as the production of metabolites that are absent in host diets or help cover energy needs (50–53), and bacterial removal may thus impair metabolism functions and ant wellbeing. Social withdrawal of unhealthy ant workers has been demonstrated for at least two ant species (54,55), and it is conceivable that the ostracism of the sick ants is driven by changes in CHCs (or other volatile compounds important in communication).…”