Abstract

BackgroundHypoxia and temperature stress are two major adverse environmental conditions often encountered by fishes. The interaction between hypoxia and temperature stresses has been well documented and oxygen is considered to be the limiting factor for the thermal tolerance of fish. Although both high and low temperature stresses can impair the cardiovascular function and the cross-resistance between hypoxia and heat stress has been found, it is not clear whether hypoxia acclimation can protect fish from cold injury.ResultsPre-acclimation of 96-hpf zebrafish larvae to mild hypoxia (5% O2) significantly improved their resistance to lethal hypoxia (2.5% O2) and increased the survival rate of zebrafish larvae after lethal cold (10°C) exposure. However, pre-acclimation of 96-hpf larvae to cold (18°C) decreased their tolerance to lethal hypoxia although their ability to endure lethal cold increased. RNA-seq analysis identified 132 up-regulated and 41 down-regulated genes upon mild hypoxia exposure. Gene ontology enrichment analyses revealed that genes up-regulated by hypoxia are primarily involved in oxygen transport, oxidation-reduction process, hemoglobin biosynthetic process, erythrocyte development and cellular iron ion homeostasis. Hypoxia-inhibited genes are enriched in inorganic anion transport, sodium ion transport, very long-chain fatty acid biosynthetic process and cytidine deamination. A comparison with the dataset of cold-regulated gene expression identified 23 genes co-induced by hypoxia and cold and these genes are mainly associated with oxidation-reduction process, oxygen transport, hemopoiesis, hemoglobin biosynthetic process and cellular iron ion homeostasis. The alleviation of lipid peroxidation damage by both cold- and hypoxia-acclimation upon lethal cold stress suggests the association of these genes with cold resistance. Furthermore, the alternative promoter of hmbsb gene specifically activated by hypoxia and cold was identified and confirmed.ConclusionsAcclimation responses to mild hypoxia and cold stress were found in zebrafish larvae and pre-acclimation to hypoxia significantly improved the tolerance of larvae to lethal cold stress. RNA-seq and bioinformatics analyses revealed the biological processes associated with hypoxia acclimation. Transcriptional events co-induced by hypoxia and cold may represent the molecular basis underlying the protection of hypoxia-acclimation against cold injury.Electronic supplementary materialThe online version of this article (doi:10.1186/s12864-015-1560-y) contains supplementary material, which is available to authorized users.

Highlights

  • Hypoxia and temperature stress are two major adverse environmental conditions often encountered by fishes

  • Hypoxia acclimation increased the cold resistance of zebrafish larvae To investigate the cross-resistance between hypoxia and cold stress, zebrafish larvae pre-acclimated to mild hypoxia or cold were exposed to lethal hypoxia and cold, respectively (Figure 1A)

  • Genes co-induced by hypoxia and cold are mainly involved in oxidation-reduction processes, hemoglobin biosynthetic process and oxygen transport

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Summary

Introduction

Hypoxia and temperature stress are two major adverse environmental conditions often encountered by fishes. The interaction between hypoxia and temperature stresses has been well documented and oxygen is considered to be the limiting factor for the thermal tolerance of fish. Temperature limits the rates of cellular biochemical reactions and dictates all aspects of fish life, including metabolism, development, growth, reproduction and behavior [1]. The acclimation of fish to thermal stresses was considered to be a process of “biochemical restructuration” [22], including synthesizing temperature specific isoenzymes [22], increasing the content of membrane lipid and the degree of fatty acid unsaturation [23], recruiting different muscle fiber types [24], generating molecular chaperones [25], and changing mitochondrial densities and their properties [26]

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