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Quantitative proteomic changes during anoxia and reoxygenation in anoxia-tolerant crucian carp

ABSTRACT: The freshwater fish crucian carp (Carassius carassius) can survive complete oxygen depletion (anoxia) for several months at low temperatures, achieved by a combination of reduced energy demand and increased glycolysis fueled by large hepatic glycogen stores. In crucian carp, the energy-requiring protein synthesis is controlled in a tissue-specific manner when oxygen levels decrease. During anoxia, translational rates are maintained at almost normoxic levels in brain, while heart and liver translation rates are strongly reduced. However, little is known about how the global proteome of these tissues are affected by oxygen variations. By applying mass spectrometry-based proteomics, 3304 proteins in brain, 3004 proteins in heart and 2516 proteins in liver were detected, of which 66 brain proteins, 243 cardiac proteins and 162 hepatic proteins were differentially expressed during the course of anoxia-reoxygenation compared to normoxic control. The brain proteome showed few differences in response to oxygen variations, indicating that anoxic survival is not regulated through protein expression in this tissue. Cardiac and hepatic adaptions to anoxia included enrichment of mitochondrial proteins involved in aerobic respiration and mitochondrial membrane integrity. We show that enzymes in the electron transport system (ETS) are regulated in a tissue-specific manner since no ETS components were regulated in brain, but were downregulated in heart and upregulated in liver during anoxia and reoxygenation. Furthermore, complement system activation was enriched in heart during anoxia. During reoxygenation, proteins involved in the cristae junction organization were regulated in the heart, possibly explaining how reactive oxygen species can be avoided when oxygen returns in this master of anoxic survival.

INSTRUMENT(S): Q Exactive

ORGANISM(S): Cyprinidae

TISSUE(S): Heart, Brain, Liver

SUBMITTER: Bernd Thiede

LAB HEAD: Anette Johansen

PROVIDER: PXD032830 | Pride | 2023-01-27

REPOSITORIES: Pride

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Project description:Intermittent hypoxia is a common stressor in estuarine and coastal habitats due to the diurnal and tidal cycles of oxygen availability. Oxygen deficiency results in energy stress by limiting aerobic ATP production, while reoxygenation may lead to oxidative injury due to the excessive production of reactive oxygen species (ROS) in mitochondria. Mitochondria are a key intracellular target of hypoxia-reoxygenation (H/R) stress due to their central role in ATP production, ROS generation and stress signaling. Marine intertidal bivalves such as the Pacific oyster Crassostrea gigas are adapted to frequent H/R cycles in the intertidal zone and maintain mitochondrial integrity and aerobic function despite frequent oxygen fluctuations. To gain insight into the molecular responses of mitochondria of the hypoxia-tolerant Pacific oyster to H/R stress, we studied changes in oxidative phosphorylation (OXPHOS) capacity, proton leak and activity of the electron transport system enzymes (ETS) in gill mitochondria of C. gigas. We furthermore investigated shifts in mitochondrial proteome and phosphoproteome after 24 h of hypoxia and 1 h of post-hypoxic recovery. Oyster mitochondria maintained normal ETS and OXPHOS capacity during H/R stress, despite a slight but significant decline in cytochrome c oxidase (Complex IV) activity after reoxygenation. Fifty total proteins and 36 phosphoproteins were differentially abundant in mitochondria of H/R exposed oysters compared with the controls. Rearrangements of the mitochondrial (phospho)proteome during H/R stress involved upregulation of mitochondrial ETS (most notably Complexes I and IV) and iron-binding proteins (frataxin and ferrochelatase) as well as suppression of the metabolic pathways that channel electrons to ubiquinone, possibly as a mechanism to limit ROS production due to the iron overload and reverse flow of electrons through ETS. H/R stress also led to upregulation of a mitophagic activator serine/threonine protein phosphatase PGAM5 and dephosphorylation of metalloendopeptidase OMA1 indicating stimulation of mitochondrial quality control mechanisms during reoxygenation. Changes in the overall abundance and phosphorylation levels of several key proteins involved in the mitochondrial protein homeostasis (including subunits of the mitochondrial ribosome, mitochondrial inner membrane translocase and elongation factor G) are consistent with the suppression of the protein synthesis during hypoxia, likely as an energy-saving mechanism. Overall, our study indicates that shifts in the mitochondrial (phospho-)proteome play an important role in responses of oysters to H/R stress and might complement adaptations of anaerobic metabolism and metabolic rate depression in ensuring hypoxic survival and rapid recovery in this hypoxia-tolerant intertidal species.

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Quantitative proteomic changes during anoxia and reoxygenation in anoxia-tolerant crucian carp

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