Surviving without oxygen involves major tissue specific changes in the proteome of crucian carp (Carassius carassius)

PeerJ. 2023 Mar 8:11:e14890. doi: 10.7717/peerj.14890. eCollection 2023.

Abstract

The crucian carp (Carassius carassius) can survive complete oxygen depletion (anoxia) for several months at low temperatures, making it an excellent model for studying molecular adaptations to anoxia. Still, little is known about how its global proteome responds to anoxia and reoxygenation. By applying mass spectrometry-based proteome analyses on brain, heart and liver tissue from crucian carp exposed to normoxia, five days anoxia, and reoxygenation, we found major changes in particularly cardiac and hepatic protein levels in response to anoxia and reoxygenation. These included tissue-specific differences in mitochondrial proteins involved in aerobic respiration and mitochondrial membrane integrity. Enzymes in the electron transport system (ETS) decreased in heart and increased massively in liver during anoxia and reoxygenation but did not change in the brain. Importantly, the data support a special role for the liver in succinate handling upon reoxygenation, as suggested by a drastic increase of components of the ETS and uncoupling protein 2, which could allow for succinate metabolism without excessive formation of reactive oxygen species (ROS). Also during reoxygenation, the levels of proteins involved in the cristae junction organization of the mitochondria changed in the heart, possibly functioning to suppress ROS formation. Furthermore, proteins involved in immune (complement) system activation changed in the anoxic heart compared to normoxic controls. The results emphasize that responses to anoxia are highly tissue-specific and related to organ function.

Keywords: Anoxia tolerance; Crucian carp; Electron transport system; Physiology; Proteomics; ROS; Reoxygenation.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Carps* / metabolism
  • Hypoxia
  • Oxygen* / metabolism
  • Proteome
  • Reactive Oxygen Species

Substances

  • Oxygen
  • Proteome
  • Reactive Oxygen Species

Grants and funding

This work was financially supported by the University of Oslo. Mass spectrometry-based proteomic analyses were performed by the Proteomics Core Facility, Department of Biosciences, University of Oslo. This facility is a member of the National Network of Advanced Proteomics Infrastructure (NAPI), which is funded by the Research Council of Norway INFRASTRUKTUR-program (project number: 295910). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.