Abstract

Mitochondria are playing key roles in setting the thermal limits of fish, but how these organelles participate in selection mechanisms during extreme thermal events associated with climate warming in natural populations is unclear. Here, we investigated the thermal effects on mitochondrial metabolism, oxidative stress, and mitochondrial gene expression in cardiac tissues of European perch (Perca fluviatilis) collected from an artificially heated ecosystem, the “Biotest enclosure”, and an adjacent reference area in the Baltic sea with normal temperatures (~ 23 °C and ~ 16 °C, respectively, at the time of capture in summer). Fish were sampled one month after a heat wave that caused the Biotest temperatures to peak at ~ 31.5 °C, causing significant mortality. When assayed at 23 °C, Biotest perch maintained high mitochondrial capacities, while reference perch displayed depressed mitochondrial functions relative to measurements at 16 °C. Moreover, mitochondrial gene expression of nd4 (mitochondrial subunit of complex I) was higher in Biotest fish, likely explaining the increased respiration rates observed in this population. Nonetheless, cardiac tissue from Biotest perch displayed higher levels of oxidative damage, which may have resulted from their chronically warm habitat, as well as the extreme temperatures encountered during the preceding summer heat wave. We conclude that eurythermal fish such as perch are able to adjust and maintain mitochondrial capacities of highly aerobic organs such as the heart when exposed to a warming environment as predicted with climate change. However, this might come at the expense of exacerbated oxidative stress, potentially threatening performance in nature.

Highlights

  • Mitochondria are playing key roles in setting the thermal limits of fish, but how these organelles participate in selection mechanisms during extreme thermal events associated with climate warming in natural populations is unclear

  • The present study characterized the thermal effects on cardiac mitochondrial metabolism, oxidative stress, and mitochondrial gene expression patterns in two nearby perch populations from thermally distinct habitats, sampled approximately one month after a severe summer heat wave

  • Our results show that perch from the Biotest enclosure generally display higher cardiac mitochondrial capacities across assay temperatures, while perch from the reference area displayed depressed mitochondrial functions when assayed at warmer temperatures

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Summary

Introduction

Mitochondria are playing key roles in setting the thermal limits of fish, but how these organelles participate in selection mechanisms during extreme thermal events associated with climate warming in natural populations is unclear. We conclude that eurythermal fish such as perch are able to adjust and maintain mitochondrial capacities of highly aerobic organs such as the heart when exposed to a warming environment as predicted with climate change This might come at the expense of exacerbated oxidative stress, potentially threatening performance in nature. Extreme temperatures (i.e., typically near an organism’s critical thermal maximum, ­CTmax) may cause protein denaturation and misassembly of mitochondrial enzymatic complexes or supercomplexes, as well as increased fluidity of mitochondrial membranes, potentially leading to subsequent loss of structural integrity, impaired kinetic properties and other mitochondrial ­dysfunctions[10,12,20,21,22,23,24] This results in sharp decreases of the reaction rates characterized by the steep descending phase of the thermal performance curve. Knowledge about mitochondrial and cellular responses to acute temperature changes in chronically warm adapted populations in nature is scant

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