Abstract
Serotonin (5-HT) is pivotal in the complex regulation of gut motility and consequent digestion of nutrients via multiple receptors. We investigated the serotonergic system in an agastric fish species, the ballan wrasse (Labrus bergylta) as it represents a unique model for intestinal function. Here we present evidence of the presence of enterochromaffin cells (EC cells) in the gut of ballan wrasse comprising transcriptomic data on EC markers like adra2a, trpa1, adgrg4, lmxa1, spack1, serpina10, as well as the localization of 5-HT and mRNA of the rate limiting enzyme; tryptophan hydroxylase (tph1) in the gut epithelium. Second, we examined the effects of dietary marine lipids on the enteric serotonergic system in this stomach-less teleost by administrating a hydrolyzed lipid bolus in ex vivo guts in an organ bath system. Modulation of the mRNA expression from the tryptophan hydroxylase tph1 (EC cells isoform), tph2 (neural isoform), and other genes involved in the serotonergic machinery were tracked. Our results showed no evidence to confirm that the dietary lipid meal did boost the production of 5-HT within the EC cells as mRNA tph1 was weakly regulated postprandially. However, dietary lipid seemed to upregulate the post-prandial expression of tph2 found in the serotonergic neurons. 5-HT in the intestinal tissue increased 3 hours after “exposure” of lipids, as was observed in the mRNA expression of tph2. This suggest that serotonergic neurons and not EC cells are responsible for the substantial increment of 5-HT after a lipid-reach “meal” in ballan wrasse. Cells expressing tph1 were identified in the gut epithelium, characteristic for EC cells. However, Tph1 positive cells were also present in the lamina propria. Characterization of these cells together with their implications in the serotonergic system will contribute to broad the scarce knowledge of the serotonergic system across teleosts.
Highlights
The gastrointestinal (GI) tract is considered a complex chemosensory system which can sense changes in gut content and release signals to the enteric nervous system (ENS) [1]
By meta-analyzing this intestinal transcriptome [from additional file 6 [3]], we wanted to first demonstrate the presence of 3 groups of genes of interest; 1) genes involved in lipid metabolism, 2) genes involved in serotonin metabolism and 3) genes considered as markers for either enterochromaffin cells (EC) cells and/or serotonergic neurons
We suggest that 1) tph1 is involved in the production of 5-HT in the gut throughout the whole trial and [2] at least part of the observed mRNA tph1 is contained in EC cells
Summary
The gastrointestinal (GI) tract is considered a complex chemosensory system which can sense changes in gut content and release signals to the enteric nervous system (ENS) [1]. The ENS is crucial for modulating gut motility (contractions and relaxations of the muscularis externa) which is required for mixing, thorough digestion of nutrients and elimination of waste products [2]. Mammals and some other higher vertebrates present two TPH isoforms; TPH1 which is found in the intestinal EC cells and TPH2 uniquely found in serotonergic neurons in both the brain and the intestine [13, 15]. Both Tph and Tph have been characterized in fish, some species have two isoforms of Tph1 [16, 17]
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