Understanding the cardiac toxicity of the anthropogenic pollutant phenanthrene on the freshwater indicator species (Salmo trutta): From whole heart to cardiomyocytes

Martins Oshioriamhe Ainerua, Jake Tinwell, Shiva Nag Kompella, Elin Sørhus, Keith N. White, Bart E. Van Dongen, Holly A. Shiels

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Abstract

Freshwater systems are faced with myriads of stressors including geomorphological alterations, nutrient overloading and pollution. Previous studies in marine fish showed polyaromatic hydrocarbons (PAHs) to be cardiotoxic. However, the cardiotoxicity of anthropogenic pollutants in freshwater fishes is unclear and has not been examined across multiple levels of cardiac organization. Here we investigated the effect of phenanthrene (Phe), a pervasive anthropogenic pollutant on a sentinel freshwater species, the brown trout (Salmo trutta). We first examined the electrical activity of the whole heart and found prolongation (∼8.6%) of the QT interval (time between ventricular depolarization and repolarization) of the electrocardiogram (ECG) and prolongation (∼13.2%) of the monophasic action potential duration (MAPD) following ascending doses of Phe. At the tissue level, Phe significantly reduced trabecular force generation by ∼24% at a concentration above 15 μM, suggesting Phe reduce cellular calcium cycling. This finding was supported by florescent microscopy showing a reduction (∼39%) in the intracellular calcium transient amplitude following Phe exposure in isolated brown trout ventricular myocytes. Single-cell electrophysiology was used to reveal the mechanism underlying both contractile and electrical dysfunctions following Phe exposure. A Phe-dependent reduction (∼38%) in the L-type Ca2+ current accounts, at least in part, for the lowered Ca2+ transient and force production. Prolongation of the MAPD and QT interval was explained by a reduction (∼70%) in the repolarising delayed rectifier K+ current following Phe exposure. Taken together, our study shows a direct impact of Phe across multiple levels of cardiac organization in a key freshwater salmonid.
Original languageEnglish
Pages (from-to)124608
JournalChemosphere
Early online date17 Aug 2019
DOIs
Publication statusPublished - 2019

Keywords

  • poly aromatic hydrocarbons
  • PAHs
  • brown trout
  • cardiac action potential
  • AP electrocardiogram
  • ECG
  • electrophysiology
  • toxicology
  • fish

Research Beacons, Institutes and Platforms

  • Sustainable Futures

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