Dual effect of metals on branchial and renal Na,K-ATPase activity in thermally acclimated crucian carp (Carassius carassius) and rainbow trout (Oncorhynchus mykiss)

Aquat Toxicol. 2023 Jan:254:106374. doi: 10.1016/j.aquatox.2022.106374. Epub 2022 Dec 16.

Abstract

Heavy metals are harmful to aquatic animals by disrupting their ionic balance. Here, we compare the effects of three metals, zinc (Zn), nickel (Ni) and manganese (Mn) on Na,K-ATPase activity in gills and kidneys in fish species with different ecophysiological characteristics. Crucian carp (Carassius carassius), a cold-dormant species, and rainbow trout (Oncorhynchus mykiss), a cold-active species, were acclimated to 2 °C and 18 °C, and branchial and renal Na,K-ATPase activities were measure in the presence of Zn, Ni and Mn. Under basal conditions, species-, tissues- and temperature-dependent differences appeared in Na,K-ATPase activity. Renal Na,K-ATPase activity was higher in trout than carp, and cold-acclimation increased Na,K-ATPase activity in both species. Cold-acclimation reduced branchial Na,K-ATPase activity in carp, but no acclimation effect was found in trout. In both species and tissues, Zn stimulated Na,K-ATPase in concentration-dependent manner at 0.1 to 3 μM. At 30 µM, Zn strongly inhibited both branchial and renal Na,K-ATPase in both species. Inhibition by Zn was stronger in trout than carp, but no differences existed between acclimation groups in either species. Ni (0.1-3.0 µM) stimulated renal Na,K-ATPase in crucian carp but not in rainbow trout. At 30 µM, Ni depressed the renal Na,K-ATPase of carp back to the control level. Mn had no statistically significant effect on Na,K-ATPase in either species. At low concentrations, Zn and Ni impose an energetic cost to fish by increasing ATP consumption in Na,K-ATPase activity. At higher concentrations, Zn, but not Ni and Mn, strongly inhibit renal and branchial Na,K-ATPase. Due to differences in baseline activity level and acclimation-induced changes in renal and branchial Na,K-ATPase, metal pollution may impair ion regulation of fish in species-specific manner and depending on season.

Keywords: Active ion pumping; Gill; Kidney; Metal pollution; Temperature acclimation.

MeSH terms

  • Animals
  • Carps* / metabolism
  • Gills
  • Kidney / metabolism
  • Metals / pharmacology
  • Oncorhynchus mykiss* / metabolism
  • Sodium / metabolism
  • Sodium-Potassium-Exchanging ATPase / metabolism
  • Water Pollutants, Chemical* / toxicity

Substances

  • Sodium-Potassium-Exchanging ATPase
  • Water Pollutants, Chemical
  • Metals
  • Sodium