Nucleobase-containing compounds evoke behavioural, olfactory, and transcriptional responses in model fishes

Angela L Shamchuk,Carlie R Lewis,Keith B Tierney,Mo Qi Wang,Danielle D Lyons,Gary Hardiman,Brian J Blunt,E Starr Hazard,Anastasia Gasheva,Kirsten Tomlin,Imogen Coe

doi:10.1139/facets-2017-0101

Angela L Shamchuk, Carlie R Lewis + Show 9 more

Open Access

https://doi.org/10.1139/facets-2017-0101

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Abstract

The sensory system of animals detects a massive and unknown array of chemical cues that evoke a diversity of physiological and behavioural responses. One group of nitrogen-containing carbon ring chemicals—nucleobases—are thought to be involved in numerous behaviours yet have received little attention. We took a top-down approach to examine responses evoked by nucleobases at behavioural, tissue, and gene expression levels. Fish generally avoided nucleobases, and this behaviour, when observed, was driven by purines but not pyrimidines. At the tissue level, olfactory neuron generator potential responses tended to be concentration specific and robust at concentrations lower than amino acid detection ranges. In terms of gene expression, more than 2000 genes were significantly upregulated following nucleobase exposure, some of which were expected (e.g., genes involved in purine binding) and some of which were not (e.g., tubulin-related genes). Humanized RNA pathway analysis showed that we had exposed the animal to a nucleobase. Our data indicate that responses to nucleobase-containing compounds may be highly structure based and are evident from changes in behaviour to mRNA expression. Many of these responses were surprising, and all provide numerous routes for further research endeavour.

Highlights

IntroductionAnimals use chemical stimuli ranging in complexity from the simple to the elaborate to facilitate activities from feeding to mating
A huge diversity of chemicals can evoke a vast array of sensory responses
Adenine was avoided at 7–10 min (p = 0.048), and a similar trend was present for adenosine at 7–10 min (p = 0.056)

Summary

Introduction

Animals use chemical stimuli ranging in complexity from the simple to the elaborate to facilitate activities from feeding to mating. One of the more intriguing classes of understudied chemical stimuli are nucleobasecontaining compounds, i.e., compounds having carbon rings with nitrogen (Table 1). Among these compounds are the sugar-containing nucleosides, which include deoxyribonucleic acids (DNA), and the phosphorylated nucleotides, which include adenosine triphosphate (ATP). Nucleotides are released by bacteria (Okabayashi et al 1963; Demain et al 1965; Saier et al 1975) and animals; the latter may excrete these compounds naturally (Murad and Pak 1972; Sato et al 1981).

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