Differences in neurochemical profiles of two gadid species under ocean warming and acidification

Abstract

BackgroundExposure to future ocean acidification scenarios may alter the behaviour of marine teleosts through interference with neuroreceptor functioning. So far, most studies investigated effects of ocean acidification on the behaviour of fish, either isolated or in combination with environmental temperature. However, only few physiological studies on this issue were conducted despite the putative neurophysiological origin of the CO2-induced behavioural changes. Here, we present the metabolic consequences of long-term exposure to projected ocean acidification (396–548 μatm PCO2 under control and 915–1272 μatm under treatment conditions) and parallel warming in the brain of two related fish species, polar cod (Boreogadus saida, exposed to 0 °C, 3 °C, 6 °C and 8 °C) and Atlantic cod (Gadus morhua, exposed to 3 °C, 8 °C, 12 °C and 16 °C). It has been shown that B. saida is behaviourally vulnerable to future ocean acidification scenarios, while G. morhua demonstrates behavioural resilience.ResultsWe found that temperature alters brain osmolyte, amino acid, choline and neurotransmitter concentrations in both species indicating thermal responses particularly in osmoregulation and membrane structure. In B. saida, changes in amino acid and osmolyte metabolism at the highest temperature tested were also affected by CO2, possibly emphasizing energetic limitations. We did not observe changes in neurotransmitters, energy metabolites, membrane components or osmolytes that might serve as a compensatory mechanism against CO2 induced behavioural impairments. In contrast to B. saida, such temperature limitation was not detected in G. morhua; however, at 8 °C, CO2 induced an increase in the levels of metabolites of the glutamate/GABA-glutamine cycle potentially indicating greater GABAergic activity in G.morhua. Further, increased availability of energy-rich substrates was detected under these conditions.ConclusionsOur results indicate a change of GABAergic metabolism in the nervous system of Gadus morhua close to the optimum of the temperature range. Since a former study showed that juvenile G. morhua might be slightly more behaviourally resilient to CO2 at this respective temperature, we conclude that the observed change of GABAergic metabolism could be involved in counteracting OA induced behavioural changes. This may serve as a fitness advantage of this respective species compared to B. saida in a future warmer, more acidified polar ocean.Electronic supplementary materialThe online version of this article (10.1186/s12983-017-0238-5) contains supplementary material, which is available to authorized users.

CO2 induced pHi changes in the brain of polar fish: a TauCEST application

“…Thus, a mixture of metabolites was analysed for 1.5°C, mimicking the intracellular composition of a polar cod brain. Intracellular concentrations of main metabolites were determined from a previous study on OA effects on neurophysiological changes in polar cod . In particular, the metabolites GABA, Gln, Glu and Tau, which were found with significant concentrations and exhibit exchangeable protons around 3.0 ppm from water, were used for the in vitro studies.…”

“…Simulations were performed by numerically solving the Bloch‐McConnell equations using a two‐pool model or a multi‐pool model for 9.4 T. The metabolites used were GABA (2.8mM), Gln (2.8mM), Glu (5mM) and Tau (20mM), which are the most prominent amino acids with exchangeable protons in the polar cod brain . The total Cr (tCr) concentration, i.e.…”

“…sum of creatine (Cr) and phosphocreatine (PCr), was assumed to be 7mM, which is a reliable concentration for a polar cod brain. This concentration was used to derive absolute values of the other metabolites, because Schmidt et al published only relative concentrations using tCr as reference …”

“…The metabolites used were GABA (2.8mM), Gln (2.8mM), Glu (5mM) and Tau (20mM), which are the most prominent amino acids with exchangeable protons in the polar cod brain. 43 The total Cr (tCr) concentration, i.e. sum of creatine (Cr) and phosphocreatine (PCr), was assumed to be 7mM, which is a reliable concentration for a polar cod brain.…”

“…This concentration was used to derive absolute values of the other metabolites, because Schmidt et al published only relative concentrations using tCr as reference. 43 The simulations used exchange rates experimentally determined by fitting the Bloch-McConnell equations, modified for a two-pool chemical exchange, to the experimental data. The calculated exchange rates for the different metabolites are shown in Table S1 of the supplementary material.…”