Impact of ocean acidification and warming on mitochondrial enzymes and membrane lipids in two Gadoid species

Abstract

Mitochondrial respiration is a multi-step pathway that involves matrix and membrane-associated enzymes and plays a key role in acclimation to variable environmental conditions, but until now it has not been clear which of these steps would be most important in acclimation to changing temperatures and CO2 levels. Considering scenarios of ocean warming and acidification we assessed the role and limitation to phenotypic plasticity in the hearts of two Gadoid species adapted to different thermal ranges: the polar cod (Boreogadus saida), an Arctic stenotherm, and the Northeast Arctic population of Atlantic cod (NEAC, Gadus morhua), a cold eurytherm. We analysed the capacity of single enzymes involved in mitochondrial respiration [citrate synthase (CS), succinate dehydrogenase (SDH), cytochrome c oxidase (CCO)], the capacity of the electron transport system and the lipid class composition of the cellular membranes. Juveniles of the two species were held for four months at four temperatures (0, 3, 6, 8 °C for polar cod and 3, 8, 12, 16 °C for NEAC), at both ambient and elevated \(P_{{{\text{CO}}_{2} }}\) (400 µatm and 1170 µatm, respectively). Polar cod showed no changes in mitochondrial enzyme capacities and in the relative lipid class composition in response to altered temperature or elevated \(P_{{{\text{CO}}_{2} }} .\) The lack of cardiac cellular plasticity together with evidence at the whole-animal level coming from other studies is indicative of little or no ability to overcome stenothermy, in particular during acclimation to 8 °C. In contrast, eurythermal NEAC exhibited modifications of membrane composition towards a more rigid structure and altered enzyme capacities to preserve functionality at higher temperatures. Furthermore, in NEAC, the capacities of SDH, CCO and CS were increased by high levels of CO2 if combined with high temperatures (12 and 16 °C), suggesting the compensation of an inhibitory effect. These results indicate that the cold eurythermal species (NEAC) is able to alter its mitochondrial function to a far greater extent than the Arctic stenotherm (polar cod), indicating greater resilience to variable environmental conditions. This difference in plasticity may underpin differences in the resilience to climate change and affect future species distributions and, eventually, survival.

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Abbreviations

NEAC:

Northeast Arctic population of Atlantic cod

RCP:

Representative concentration pathway

CS:

Citrate synthase

CCO:

Cytochrome c oxidase

SDH:

Succinate dehydrogenase

CI:CIII:

NADH:cytochrome c oxidoreductase

Chol:

Cholesterol

PE:

Phosphatidylethanolamine

PC:

Phosphatidylcholine

TCA cycle:

Tricarboxylic acid cycle

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Acknowledgements

We thank Silvia Hardenberg, Timo Hirse, Isabel Ketelsen, Nils Koschnick, Kristina Kunz, Matthias Schmidt and Heidrun Windisch for their help during the incubation and sampling and Dieter Janssen and Valeria Adrian for their assistance during the lipid extraction and analysis. Furthermore, we acknowledge the Project Polarisation (Norwegian Research Council, 214184/F20) for providing polar cod specimens and the crews of RV Heincke (HE 408) and RV Helmer Hanssen (University of Tromsø) for the animal collection. This study was supported by the German Federal Ministry of Education and Research (BMBF, FKZ 03F0655B, FKZ 03F0728B) within the Research Program BIOACID Phase II and by the PACES Program of AWI.

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Correspondence to Felix C. Mark.

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The handling of the specimens of polar cod and NEAC was carried out according to the Ethical Permission Number AZ522-27–22/02–00 (113) released by the Senator for Healthcare, Bahnhofsplatz 29, 28195 Bremen on February 21st, 2013 (permit valid until February 21st, 2018).

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This article belongs to the special issue on the “Arctic Gadids in a Changing Climate”, coordinated by Franz Mueter, Haakon Hop, Benjamin Laurel, Caroline Bouchard, and Brenda Norcross.

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Leo, E., Graeve, M., Storch, D. et al. Impact of ocean acidification and warming on mitochondrial enzymes and membrane lipids in two Gadoid species. Polar Biol 43, 1109–1120 (2020). https://doi.org/10.1007/s00300-019-02600-6

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Keywords

  • Atlantic cod
  • Climate change
  • Lipid class
  • Metabolism
  • Mitochondria
  • Polar cod
  • Mitochondrial enzyme