The Metabolomic Response of Crucian Carp (<i>Carassius carassius)</i> to Anoxia and Reoxygenation Differs between Tissues and Hints at Uncharacterized Survival Strategies

The anoxia-tolerant crucian carp (<i>Carassius carassius</i>) has been studied in detail for numerous years, with particular focus on unravelling the underlying physiological mechanisms of anoxia tolerance. However, relatively little work has been focused on what occurs beyond anoxia, an...

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Main Authors: Helge-Andre Dahl, Anette Johansen, Göran E. Nilsson, Sjannie Lefevre
Format: Article
Language:English
Published: MDPI AG 2021-07-01
Series:Metabolites
Subjects:
Online Access:https://www.mdpi.com/2218-1989/11/7/435
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author Helge-Andre Dahl
Anette Johansen
Göran E. Nilsson
Sjannie Lefevre
author_facet Helge-Andre Dahl
Anette Johansen
Göran E. Nilsson
Sjannie Lefevre
author_sort Helge-Andre Dahl
collection DOAJ
description The anoxia-tolerant crucian carp (<i>Carassius carassius</i>) has been studied in detail for numerous years, with particular focus on unravelling the underlying physiological mechanisms of anoxia tolerance. However, relatively little work has been focused on what occurs beyond anoxia, and often the focus is a single organ or tissue type. In this study, we quantified more than 100 metabolites by capillary electrophoresis-mass spectrometry (CE-MS) in brain, heart, liver, and blood plasma from four experimental groups, being normoxic (control) fish, anoxia-exposed fish, and two groups that had been exposed to anoxia followed by reoxygenation for either 3 h or 24 h. The heart, which maintains cardiac output during anoxia, unexpectedly, was slower to recover compared to the brain and liver, mainly due to a slower return to control concentrations of the energy-carrying compounds ATP, GTP, and phosphocreatine. Crucian carp accumulated amino acids in most tissues, and also surprisingly high levels of succinate in all tissues investigated during anoxia. Purine catabolism was enhanced, leading to accumulation of uric acid during anoxia and increasing urea formation that continued into 24 h of reoxygenation. These tissue-specific differences in accumulation and distribution of the metabolites may indicate an intricate system of transport between tissues, opening for new avenues of investigation of possible mechanisms aimed at reducing the generation of reactive oxygen species (ROS) and resultant tissue damage during reoxygenation.
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spelling doaj.art-fa20be0b942a404dbf45cd976bf9c1122023-11-22T04:22:43ZengMDPI AGMetabolites2218-19892021-07-0111743510.3390/metabo11070435The Metabolomic Response of Crucian Carp (<i>Carassius carassius)</i> to Anoxia and Reoxygenation Differs between Tissues and Hints at Uncharacterized Survival StrategiesHelge-Andre DahlAnette JohansenGöran E. Nilsson0Sjannie Lefevre1Section for Physiology and Cell Biology, Department of Biosciences, University of Oslo, 0371 Oslo, NorwaySection for Physiology and Cell Biology, Department of Biosciences, University of Oslo, 0371 Oslo, NorwayThe anoxia-tolerant crucian carp (<i>Carassius carassius</i>) has been studied in detail for numerous years, with particular focus on unravelling the underlying physiological mechanisms of anoxia tolerance. However, relatively little work has been focused on what occurs beyond anoxia, and often the focus is a single organ or tissue type. In this study, we quantified more than 100 metabolites by capillary electrophoresis-mass spectrometry (CE-MS) in brain, heart, liver, and blood plasma from four experimental groups, being normoxic (control) fish, anoxia-exposed fish, and two groups that had been exposed to anoxia followed by reoxygenation for either 3 h or 24 h. The heart, which maintains cardiac output during anoxia, unexpectedly, was slower to recover compared to the brain and liver, mainly due to a slower return to control concentrations of the energy-carrying compounds ATP, GTP, and phosphocreatine. Crucian carp accumulated amino acids in most tissues, and also surprisingly high levels of succinate in all tissues investigated during anoxia. Purine catabolism was enhanced, leading to accumulation of uric acid during anoxia and increasing urea formation that continued into 24 h of reoxygenation. These tissue-specific differences in accumulation and distribution of the metabolites may indicate an intricate system of transport between tissues, opening for new avenues of investigation of possible mechanisms aimed at reducing the generation of reactive oxygen species (ROS) and resultant tissue damage during reoxygenation.https://www.mdpi.com/2218-1989/11/7/435metabolomicsglycolysiselectron transport chainfumaratesuccinatealternative electron acceptor
spellingShingle Helge-Andre Dahl
Anette Johansen
Göran E. Nilsson
Sjannie Lefevre
The Metabolomic Response of Crucian Carp (<i>Carassius carassius)</i> to Anoxia and Reoxygenation Differs between Tissues and Hints at Uncharacterized Survival Strategies
Metabolites
metabolomics
glycolysis
electron transport chain
fumarate
succinate
alternative electron acceptor
title The Metabolomic Response of Crucian Carp (<i>Carassius carassius)</i> to Anoxia and Reoxygenation Differs between Tissues and Hints at Uncharacterized Survival Strategies
title_full The Metabolomic Response of Crucian Carp (<i>Carassius carassius)</i> to Anoxia and Reoxygenation Differs between Tissues and Hints at Uncharacterized Survival Strategies
title_fullStr The Metabolomic Response of Crucian Carp (<i>Carassius carassius)</i> to Anoxia and Reoxygenation Differs between Tissues and Hints at Uncharacterized Survival Strategies
title_full_unstemmed The Metabolomic Response of Crucian Carp (<i>Carassius carassius)</i> to Anoxia and Reoxygenation Differs between Tissues and Hints at Uncharacterized Survival Strategies
title_short The Metabolomic Response of Crucian Carp (<i>Carassius carassius)</i> to Anoxia and Reoxygenation Differs between Tissues and Hints at Uncharacterized Survival Strategies
title_sort metabolomic response of crucian carp i carassius carassius i to anoxia and reoxygenation differs between tissues and hints at uncharacterized survival strategies
topic metabolomics
glycolysis
electron transport chain
fumarate
succinate
alternative electron acceptor
url https://www.mdpi.com/2218-1989/11/7/435
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