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Independent effects of seawater pH and high P-CO2 on olfactory sensitivity in fish: possible role of carbonic anhydrase

Publication . Velez, Zélia; Costa, Rita; Wang, Wenjing; Hubbard, Peter

Ocean acidificationmay alter olfactory-driven behaviour in fish by direct effects on the peripheral olfactory system; olfactory sensitivity is reduced in CO2-acidified seawater. The current study tested whether this is due to elevated P-CO2 or the consequent reduction in seawater pH and, if the former, the possible involvement of carbonic anhydrase, the enzyme responsible for the hydration of CO2 and production of carbonic acid. Olfactory sensitivity to amino acids was assessed by extracellularmulti-unit recording from the olfactory nerve of the gilthead seabream (Sparus aurata L.) in normal seawater (pH similar to 8.2), and after acute exposure to acidified seawater (pH similar to 7.7) but normal P-CO2 (similar to 340 mu atm) or to high P-CO2 seawater (similar to 1400 mu atm) at normal pH (similar to 8.2). Reduced pH in the absence of elevated P-CO2 caused a reduction in olfactory sensitivity to L-serine, L-leucine, L-arginine and L-glutamine, but not L-glutamic acid. Increased P-CO2 in the absence of changes in pH caused reduced olfactory sensitivity to L-serine, L-leucine and L-arginine, including increases in their threshold of detection, but had no effect on sensitivity to L-glutamine and L-glutamic acid. Inclusion of 1 mmol l(-1) acetazolamide (a membrane-permeant inhibitor of carbonic anhydrase) in the seawater reversed the inhibition of olfactory sensitivity to L-serine caused by high P-CO2. Ocean acidification may reduce olfactory sensitivity by reductions in seawater pH and intracellular pH (of olfactory receptor neurones); the former by reducing odorant-receptor affinity, and the latter by reducing the efficiency of olfactory transduction. The physiological role of carbonic anhydrase in the olfactory receptor neurones remains to be explored.

2021-03Journal article

Open Access

Short- and medium-term exposure to ocean acidification reduces olfactory sensitivity in Gilthead Seabream

Publication . Velez, Zélia; Roggatz, Christina C.; Benoit, David M.; Hardege, Jörg D.; Hubbard, Peter

The effects of ocean acidification on fish are only partially understood. Studies on olfaction are mostly limited to behavioral alterations of coral reef fish; studies on temperate species and/or with economic importance are scarce. The current study evaluated the effects of short- and medium-term exposure to ocean acidification on the olfactory system of gilthead seabream (Spares aurata), and attempted to explain observed differences in sensitivity by changes in the protonation state of amino acid odorants. Short-term exposure to elevated PCO2 decreased olfactory sensitivity to some odorants, such as L-serine, L-leucine, L-arginine, L-glutamate, and conspecific intestinal fluid, but not to others, such as L-glutamine and conspecific bile fluid. Seabream were unable to compensate for high PCO2 levels in the medium term; after 4 weeks exposure to high PCO2 , the olfactory sensitivity remained lower in elevated PCO2 water. The decrease in olfactory sensitivity in high PCO2 water could be partly attributed to changes in the protonation state of the odorants and/or their receptor(s); we illustrate how protonation due to reduced pH causes changes in the charge distribution of odorant molecules, an essential component for ligand-receptor interaction. However, there are other mechanisms involved. At a histological level, the olfactory epithelium contained higher densities of mucus cells in fish kept in high CO2 water, and a shift in pH of the mucus they produced to more neutral. These differences suggest a physiological response of the olfactory epithelium to lower pH and/or high CO2 levels, but an inability to fully counteract the effects of acidification on olfactory sensitivity. Therefore, the current study provides evidence for a direct, medium term, global effect of ocean acidification on olfactory sensitivity in fish, and possibly other marine organisms, and suggests a partial explanatory mechanism.

2019-07-03Journal article

Open Access

Ocean acidification affects the expression of neuroplasticity and neuromodulation markers in seabream

Publication . A Costa, Rita; Olvera, Aurora; Power, Deborah Mary; Velez, Zélia

A possible explanation for acidification-induced changes in fish behaviour is that acidification interferes with neurogenesis and modifies the plasticity of neuronal circuitry in the brain. We tested the effects on the olfactory system and brain of gilthead seabream (Sparus aurata) to 4 weeks' exposure to ocean acidification (OA). Olfactory epithelium (OE) morphology changed shortly after OA exposure and persisted over the 4 weeks. Expression of genes related to olfactory transduction, neuronal excitability, synaptic plasticity, GABAergic innervation, and cell proliferation were unchanged in the OE and olfactory bulb (OB) after 4 weeks' exposure. Short-term changes in the ionic content of plasma and extradural fluid (EDF) returned to control levels after 4 weeks' exposure, except for [Cl-], which remained elevated. This suggests that, in general, there is an early physiological response to OA and by 4 weeks a new homeostatic status is achieved. However, expression of genes involved in proliferation, differentiation and survival of undifferentiated neurons were modified in the brain. In the same brain areas, expression of thyroid hormone signalling genes was altered suggesting modifications in the thyroid-system may be linked to the changes in neuroplasticity and neurogenesis. Overall, the results of the current study are consistent with and effect of OA on neuroplasticity.

2022-03Journal article

Open Access

GABA receptors in the olfactory epithelium of the gilthead seabream (Sparus aurata)

Publication . Costa, Rita; Velez, Zélia; Hubbard, Peter

Exposure to high PCO2/low pH seawater induces behavioural alterations in fish; a possible explanation for this is a reversal of Cl-/HCO3- currents through GABAA receptors (the GABAA receptor theory). However, the main evidence for this is that gabazine, a GABAA receptor antagonist, reverses these effects when applied to the water, assuming that exposure to systems other than the CNS would be without effect. Here, we show the expression of both metabotropic and ionotropic GABA receptors, and the presence of GABAA receptor protein, in the olfactory epithelium of gilthead seabream. Furthermore, exposure of the olfactory epithelium to muscimol (a specific GABAA receptor agonist) increases or decreases the apparent olfactory sensitivity to some odorants. Thus, although the exact function of GABAA receptors in the olfactory epithelium is not yet clear, this may complicate the interpretation of studies wherein water-borne gabazine is used to reverse the effects of high CO2 levels on olfactory-driven behaviour in fish.

2022Journal article

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