Seasonal remodelling of the fish heart alters sensitivity to petrochemical pollutant, 3-methylphenanthrene

Exploitation of offshore oil reserves, heightened traffic in marine transportation routes, and the release of petrochemicals from the thawing of permafrost and glaciers is increasing the bioavailability of polycyclic aromatic hydrocarbons (PAHs) to aquatic organisms. This availability may also change with the seasons as temperature changes accessibility of Arctic transport routes and the degree of land- and ice-melt and thus run-off into coastal ecosystems. Seasonal temperature change also remodels the ion channels in the heart of fish to facilitated preserved cardiac function across a range of temperatures. How this seasonal cardiac remodelling impacts vulnerability to pollutants is currently unknown. In this study we accessed the electrical activity of navaga cod (Eleginus nawaga) ventricular cardiomyocytes under the dual influence of seasonal change and varying concentrations of a pervasive PAH pollutant, 3-methylphenanthrene (3-MP). We used whole-cell patch-clamp to elucidate the effect of various doses of 3-MP on action potential (AP) parameters and the main ion currents (I_Kr, I_K1, I_Na, I_Ca) in ventricular cardiomyocytes isolated from navaga cod in winter and summer at the White Sea, close to the Russian Arctic circle. Navaga cod ventricular cardiomyocytes were particularly vulnerable to 3-MP during the winter season. Exposure to 300 nM 3-MP resulted in significant changes in AP duration in winter-acclimatized fish, whereas no such changes were observed in summer-acclimatized fish. The I_Kr current was the most sensitive to 3-MP, with a winter IC₅₀ of 49.7 nM and a summer IC₅₀ of 53 μM. The I_Na current also exhibited seasonal shifts in sensitivity to 3-MP, with IC₅₀ values of 2.39 μM in winter-acclimatized fish and 7.73 μM in summer-acclimatized fish. No significant differences were observed in the effect of 3-MP on the peak I_Ca current, although 3 μM of 3-MP caused a pronounced decrease in charge transferred by I_Ca (e.g. Q_Ca) in both seasons. The I_K1 current was insensitive to 3-MP in both winter and summer fish. These findings highlight how remodelling of the fish heart with changing season alters the potency of PAH pollution. This paper lays the groundwork for future research on the molecular mechanisms that drive the altered seasonal potency of pollutants in navaga cod and other species.