The dominant detritus‐feeding invertebrate in Arctic peat soils derives its essential amino acids from gut symbionts

Abstract

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 have 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 fibre diets, whereas most of the enchytraeids' EAA derived from dietary sources when fed on lower fibre diets. Our gene sequencing results of gut microbiota showed that the worms harbour 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 demonstrates that symbiotic bacteria in the gut lumen appear to function as partners both for symbiotic EAA supplementation and for digestion of insoluble plant fibres.

Compound‐specific isotope analysis of amino acids as a new tool to uncover trophic chains in soil food webs

“…, Larsen et al. ) in that the studied consumers were depleted rather than enriched relative to food resources. Symbiotic supplementation usually leads to enriched 13 C values in hosts because of respiration of isotopically light CO 2 (McConnaughey et al.…”

“…, Larsen et al. ). However, in the latter studies, 13 C offsets among multiple eAAs between consumers and their food resources varied among different consumer–resource relationships, indicating that there is a need for controlled feeding experiments on a wider range of taxa, specifically testing persistence of eAA fingerprints from dietary protein into consumer tissue (Whiteman et al.…”

“…, Larsen et al. ). Feeding studies with fungi, bacteria, and animal consumers suggest that CSIA treats microorganisms as trophic analogs of animals, thus identifying trophic positions of decomposers while accounting for microbial contribution to their diet (Steffan et al.…”

“…Fingerprinting has been successfully used to determine basal resources of, e.g., butterflies and fruit flies (Larsen et al 2009), Daphnia, mussels and fish (Larsen et al 2013), and turtles (Arthur et al 2014). Due to cryptic lifestyles and variable microbial contributions to the diet, fingerprinting can be most useful for soil-living species; it has been used already to differentiate food sources of earthworms and enchytraeids (Larsen et al 2016a, Potapov et al 2019a) and to uncover eAA supplementation from gut microbes to consumers (Ayayee et al 2016, Larsen et al 2016b). However, in the latter studies, 13 C offsets among multiple eAAs between consumers and their food resources varied among different consumer-resource relationships, indicating that there is a need for controlled feeding experiments on a wider range of taxa, specifically testing persistence of eAA fingerprints from dietary protein into consumer tissue (Whiteman et al 2019).…”

Biotic interactions and trait-based ecosystem functioning in soil

“…Our understanding of collembolan feeding habits at the species or functional group level is steadily increasing (Chamberlain et al, 2006;Ngosong et al, 2011;Ruess et al, 2007;Sechi et al, 2014a), but several gaps still exist. It is known that Collembola are closely associated with the rhizosphere food web being nutritionally supported by root-derived resources (Endlweber et al, 2009;Larsen et al, 2007;Sabais et al, 2012Larsen et al 2016b), but the path through which they obtain these resources is not yet clear. While euedaphic and hemiedaphic species have been shown to incorporate recent photosynthate carbon (C) from crops (Larsen et al, 2007;Ostle et al, 2007), A.M. recently demonstrated that only a fraction of these plant derived resources derives from direct foraging on roots.…”