Exploring the potential for an evolutionarily conserved role of the taste 1 receptor gene family in gut sensing mechanisms of fish

Anna Rita Angotzi; Esther Leal; Sara Puchol; José M Cerdá-Reverter; Sofia Morais

doi:10.1016/j.aninu.2022.08.010

Exploring the potential for an evolutionarily conserved role of the taste 1 receptor gene family in gut sensing mechanisms of fish

Anim Nutr. 2022 Aug 31:11:293-308. doi: 10.1016/j.aninu.2022.08.010. eCollection 2022 Dec.

Authors

Anna Rita Angotzi¹, Esther Leal¹, Sara Puchol¹, José M Cerdá-Reverter¹, Sofia Morais²

Affiliations

¹ Department of Fish Physiology and Biotechnology, Instituto de Acuicultura de Torre de la Sal, IATS-CSIC, Torre la Sal s/n, Ribera de Cabanes, 12595 Castellon, Spain.
² Lucta S.A., Innovation Division, Animal Science Unit, UAB Research Park, 08193 Bellaterra, Spain.

Abstract

In this study, we investigated the transcriptional spatio-temporal dynamics of the taste 1 receptor (T1R) gene family repertoire in seabream (Sparus aurata [sa]), during larval ontogeny and in adult tissues. In early larval development, saT1R expression arises heterochronously, i.e. the extraoral taste-related perception in the gastrointestinal tract (GIT) anticipates first exogenous feeding (at 9 days post hatching [dph]), followed by the buccal/intraoral perception from 14 dph onwards, supporting the hypothesis that the early onset of the molecular machinery underlying saT1R expression in the GIT is not induced by food but rather genetically hardwired. During adulthood, we characterized the expression patterns of sa T1R within specific tissues (n = 4) distributed in oropharingeal, GIT and brain regions substantiating their functional versatility as chemosensory signaling players to a variety of biological functions beyond oral taste sensation. Further, we provided for the first time direct evidences in fish for mRNA co-expression of a subset of saT1R genes (mostly sa T1R3, i.e. the common subunit of the heterodimeric T1R complexes for the detection of "sweet" and "umami" substances), with the selected gut peptides ghrelin (ghr), cholecystokinin (cck), hormone peptide yy (pyy) and proglucagon (pg). Each peptide defines the enteroendocrine cells (ECCs) identity, and establishes on morphological basis, a direct link for T1R chemosensing in the regulation of fish digestive processes. Finally, we analyzed the spatial gene expression patterns of 2 taste signaling components functionally homologous to the mammalian G(i)α subunit gustducin, namely sa G( i )α1 and sa G( i )α2, and demonstrated their co-localization with the saT1R3 in EECs, thus validating their direct involvement in taste-like transduction mechanisms of the fish GIT. In conclusion, data provide new insights in the evolutionary conservation of gut sensing in fish suggesting a conserved role for nutrient sensors modulating entero-endocrine secretion.

Keywords: Fish larvae; G(i) alpha protein subunits 1 and 2; Gut nutrient sensing; Gut peptides; Taste 1 receptor.