Taste beyond oral perception in seabream sparus aurata: new evidence for functional gut chemical sensing in fish

Abstract

[Introduction]: Taste receptors (TRs) are classically associated to the perception of gustatory sensations in oral tissues. However, many TRs are also found in different body tissues including the gastrointestinal tract (GIT), where they perform important roles (Finger and Kinnamon, 2011). In the GIT, the presence of TRs in specialized cells (enteroendocrine cells: EECs) regulates digestive, absorptive and metabolic functions through gut sensing mechanisms (Alpers, 2010). Functional actions of TRs are associated to their co-expression with gut peptides, including ghrelin (GHR), cholecystokinin (CCK), glucagon-like peptide-1 (GLP-1) or peptide YY (PYY), to cite a few. Once a TR is activated, an intracellular signaling cascade is initiated, terminating with peptide secretion in the EEC basolateral side, which can signal neighboring (paracrine action) or remote (endocrine action) cells, or activate afferent neurons (neural action). The taste receptor type 1 (T1R) family is one of the TR types that is commonly expressed in EECs, acting as heterodimeric sensors of nutrients in the mammalian gut: T1R1/ T1R3 responding to umami compounds such as amino acids, and T1R2/T1R3 to sweet substances. We previously showed the expression of the Sparus aurata (sa) T1R gene repertoire in oropharyngeal, GIT and brain tissues. However, this does not necessarily imply a conserved role in gut sensing. Furthermore, expression in GIT was observed in early larval stages but no expression was found in oropharyngeal tissues up to 12 days post-hatching (dph), which was puzzling. The present study aimed to provide direct evidence for mRNAs co-expression of saT1R genes (mostly t1r3, as the common element of both receptors) with EEC-type peptides such as ghr, cck, pyy and proglucagon (pg), to establish a morphological link indicating possible roles of T1R in gut nutrient-sensing mechanisms and in the regulation of fish digestive processes. A second objective was to extend the period of investigation during larval ontogeny to establish the temporal pattern of expression in GIT and oral tissues for the entire saT1R gene repertoire in relation to first-feeding.