The dominant detritus-feeding invertebrate in Arctic peat soils derives its essential amino acids from gut symbionts.
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.
Department of Agroecology, Faculty of Sciences and Technology, Aarhus University, Blichers Allé, Postbox 50, 8830, Tjele, Denmark.|Leibniz-Laboratory for Radiometric Dating and Stable Isotope Research, Christian-Albrechts-Universität zu Kiel, 24118, Kiel, Germany.
Thomas
0000-0002-0311-9707
T
Larsen
Integrative Freshwater Ecology Group, Centre for Advanced Studies of Blanes (CEAB), Spanish Research Council (CSIC), 17300 Blanes, Catalonia, Spain.
Marc
M
Ventura
Department of Agroecology, Faculty of Sciences and Technology, Aarhus University, Blichers Allé, Postbox 50, 8830, Tjele, Denmark.
Kristine
K
Maraldo
Integrative Freshwater Ecology Group, Centre for Advanced Studies of Blanes (CEAB), Spanish Research Council (CSIC), 17300 Blanes, Catalonia, Spain.
Xavier
X
Triadó-Margarit
Integrative Freshwater Ecology Group, Centre for Advanced Studies of Blanes (CEAB), Spanish Research Council (CSIC), 17300 Blanes, Catalonia, Spain.
Emilio O
EO
Casamayor
Leibniz-Laboratory for Radiometric Dating and Stable Isotope Research, Christian-Albrechts-Universität zu Kiel, 24118, Kiel, Germany.
Yiming V
YV
Wang
Leibniz-Laboratory for Radiometric Dating and Stable Isotope Research, Christian-Albrechts-Universität zu Kiel, 24118, Kiel, Germany.
Nils
N
Andersen
Institute of Arctic Biology and Department of Biology and Wildlife, University of Alaska Fairbanks, Fairbanks, AK, 99775-7000, USA.
Diane M
DM
O'Brien
D000413:Alaska; D000601:Amino Acids, Essential / Q000378:metabolism*; D000818:Animals; D001110:Arctic Regions; D001419:Bacteria / Q000145:classification / Q000235:genetics; D004032:Diet; D000069196:Gastrointestinal Microbiome; D009835:Oligochaeta / Q000382:microbiology* / Q000502:physiology*; D012329:RNA, Bacterial / Q000235:genetics; D012336:RNA, Ribosomal, 16S / Q000235:genetics; D017423:Sequence Analysis, RNA; D013559:Symbiosis
D000601:Amino Acids, Essential; D012329:RNA, Bacterial; D012336:RNA, Ribosomal, 16S
Annelids; Chthoniobacterales; Flammeovirgaceae; nutritional symbiosis; oligochaetes; soil food web; white potworms