Microbiota-Dependent and -Independent Production of l-Dopa in the Gut of Daphnia magna

Host-microbiome interactions are essential for the physiological and ecological performance of the host, yet these interactions are challenging to identify. Neurotransmitters are commonly implicated in these interactions, but we know very little about the mechanisms of their involvement, especially in invertebrates. Here, we report a peripheral catecholamine (CA) pathway involving the gut microbiome of the model species Daphnia magna. We demonstrate the following: (i) tyrosine hydroxylase and Dopa (3,4-dihydroxyphenylalanine) decarboxylase enzymes are present in the gut wall; (ii) Dopa decarboxylase gene is expressed in the gut by the host, and its expression follows the molt cycle peaking after ecdysis; (iii) biologically active l-Dopa, but not dopamine, is present in the gut lumen; (iv) gut bacteria produce l-Dopa in a concentration-dependent manner when provided l-tyrosine as a substrate. Impinging on gut bacteria involvement in host physiology and ecologically relevant traits, we suggest l-Dopa as a communication agent in the host-microbiome interactions in daphnids and, possibly, other crustaceans. IMPORTANCE Neurotransmitters are commonly implicated in host-microbiome communication, yet the molecular mechanisms of this communication remain largely elusive. We present novel evidence linking the gut microbiome to host development and growth via neurotransmitter l-Dopa in Daphnia, the established model species in ecology and evolution. We found that both Daphnia and its gut microbiome contribute to the synthesis of the l-Dopa in the gut. We also identified a peripheral pathway in the gut wall, with a molt stage-dependent dopamine synthesis, linking the gut microbiome to the daphnid development and growth. These findings suggest a central role of l-Dopa in the bidirectional communication between the animal host and its gut bacteria and translating into the ecologically important host traits suitable for subsequent testing of causality by experimental studies.