Supplementation of nutrients by symbionts enables consumers to thrive on resources that might otherwise be insufficient to meet nutritional demands. Such nutritional subsidies by intracellular symbionts has been well studied; however, supplementation of de novo synthesized nutrients to hosts by extracellular gut symbionts is poorly documented, especially for generalists with relatively undifferentiated intestinal tracts. Although gut symbionts facilitate degradation of resources that would otherwise remain inaccessible to the host, such digestive actions alone cannot make up for dietary insufficiencies of macronutrients such as essential amino acids (EAA). Documenting whether gut symbionts also function as partners for symbiotic EAA supplementation is important because the question of how some detritivores are able to subsist on nutritionally insufficient diets has remained unresolved. To answer this poorly-understood nutritional aspect of symbiont-host interactions, we studied the enchytraeid worm, a bulk soil feeder that thrives in arctic peatlands. In a combined field and laboratory study, we employed stable isotope fingerprinting of amino acids to identify the biosynthetic origins of amino acids to bacteria, fungi and plants in enchytraeids. Enchytraeids collected from arctic peatlands derived more than 80% of their EAA from bacteria. In a controlled feeding study with the enchytraeid Enchytraeus crypticus, EAA derived almost exclusively from gut bacteria when the worms fed on higher fiber diets, whereas most of the enchytraeids' EAA derived from dietary sources when fed on lower fiber diets. Our gene sequencing results of gut microbiota showed that the worms harbor several taxa in their gut lumen absent from their diets and substrates. Almost all gut taxa are candidates for EAA supplementation because almost all belong to clades capable of biosynthesizing EAA. Our study provides the first evidence of extensive symbiotic supplementation of EAA by microbial gut symbionts, and demonstrate that symbiotic bacteria in the gut lumen appear to function as partners for both symbiotic EAA supplementation as well as for digestion of insoluble plant fibers.

13C values of amino acids Sample 13C values (‰) of amino acids. Each sample was analyzed in triplicate (mean ± SD). NA indicates missing values or replicates. The values are compiled from this study and Larsen et al. (Plos One 2013) (marked with asterisk under sample code). Larsen_13CAA.csv

Peer reviewed