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Effect of acute hypoxia on the brain energy metabolism of the scorpionfish Scorpaena porcus Linnaeus, 1758: the pattern of oxidoreductase activity and adenylate system

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Abstract

The activity of oxidoreductases, malate dehydrogenase and lactate dehydrogenase (MDH, 1.1.1.37; LDH, 1.1.1.27), as well as parameters of adenylate system—[ATP], [ADP], [AMP], total adenylate pool (AP), and adenylate energy charge (AEC) in medulla oblongata (MB) and forebrain, midbrain, and diencephalon (FDMB)—were studied in the scorpionfish under acute hypoxia (0.9–1.2 mg O2·L−1, 90 min). A higher MDH activity level was observed in MB and FDMB, as compared to LDH (p < 0.05). At the same time, MB showed a higher adenylate content and increased AP (p < 0.05). AEC did not exceed ~ 0.7 (vs. the maximum of this index ~ 0.9–1.0) in the brain of the scorpionfish indicating adaptation of the tissue energy status to hypoxia. A rapid decrease in MDH activity (p < 0.05) was observed in MB under acute hypoxia. These changes were accompanied by insignificant LDH activation. A pronounced LDH activation (p < 0.05), a decrease in MDH activity, and the highest AP raise (p < 0.05) were observed in FDMB, suggesting activation of glycolysis and simultaneous decrease in the rate of ATP consumption. MB and FDMB demonstrated the ability to a relative retention of AEC during hypoxia. The unidirectional metabolic adaptation was based on the intensification of glycolysis, a decrease of ATP consumption, and a subsequent increase in adenylate concentration that allowed the scorpionfish brain structures to maintain the energy status under acute hypoxia.

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Funding

This study was funded by A.O. Kovalevsky Institute of Biology of the Southern Seas of Russian Academy of Sciences (reg. no. 121041400077–1), and partial financial support was received from the grant of Russian Foundation of Basic Research (reg. no. 20–44-920001).

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E.E.K. set the tasks, performed preparation of fish heart chambers and statistical data processing, and wrote and edited the manuscript; A.A.S. offered a pivotal idea, set the tasks and experimental design, and wrote and edited the manuscript; I.V.G. performed the assay of enzyme activities and statistical data processing, prepared illustrations, and wrote and edited the manuscript; I.V.S. and A.A.S. performed the assay of adenyl nucleotides and statistical data processing. All authors read and approved the final manuscript.

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Correspondence to Evgenia E. Kolesnikova.

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All procedures using fish were accomplished in accordance with the European Communities Council Directive (2010/63/EU) and approved by the local Institutional Animal Care and Use Committee (protocol #28 from 15.02. 2018).

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The authors declare no competing interests.

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Kolesnikova, E.E., Soldatov, A.A., Golovina, I.V. et al. Effect of acute hypoxia on the brain energy metabolism of the scorpionfish Scorpaena porcus Linnaeus, 1758: the pattern of oxidoreductase activity and adenylate system. Fish Physiol Biochem 48, 1105–1115 (2022). https://doi.org/10.1007/s10695-022-01103-2

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  • DOI: https://doi.org/10.1007/s10695-022-01103-2

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