Nutritional roles of gut symbionts in an herbivorous ant Cephalotes varians

Many of the earth’s most marginal niches have been successfully colonized by eukaryotes only with the aid of symbiosis. Ants in rainforest canopies occupy such a marginal niche, as prey biomass appears insufficient to support the biomass of the dominant ant fauna. When combined with evidence for carbon rich and nitrogen poor diets of many arboreal ants, this leads to a hypothesis that these ants have thrived within their inhospitable canopy niches due to nutritional contributions of microbial symbionts. Here we applied experimental and metagenomic approaches to assess symbiont-mediated roles in nitrogen metabolism for an herbivorous arboreal ant, Cephalotes varians. Experimental measures of nutritional contributions to nitrogen recycling demonstrated that gut symbionts of C. varians incorporate nitrogen from urea into amino acids for their host ants. Metagenomic analyses further confirmed the symbionts’ contribution to host nutrition through recycling of nitrogenous wastes and biosynthesis of amino acids. Unlike obligate bacteriocyte-dwelling symbionts, nitrogen provisioning in the Cephalotes system involves both essential and non-essential amino acids, with key steps of nitrogen metabolic pathways being shared among several extracellular gut symbionts. While only Burkholderiales associates can convert uric acid-derived host wastes to urea, multiple speciesuse urea to derive precursors for amino acid biosynthesis—a function carried out by most of the dominant symbiotic taxa in C. varians guts. Taken together, our findings provide the second evidence for nutritional contributions by symbiotic bacteria of herbivorous ants, adding strong support to the hypothesis that symbionts have a major role in the success of arboreal ant herbivores.