Liver transcriptome analysis in gilthead sea bream upon exposure to low temperature

Abstract

BackgroundWater temperature greatly influences the physiology and behaviour of teleost fish as other aquatic organisms. While fish are able to cope with seasonal temperature variations, thermal excursions outside their normal thermal range might exceed their ability to respond leading to severe diseases and death.Profound differences exist in thermal tolerance across fish species living in the same geographical areas, promoting for investigating the molecular mechanisms involved in susceptibility and resistance to low and high temperatures toward a better understanding of adaptation to environmental challenges. The gilthead sea bream, Sparus aurata, is particularly sensitive to cold and the prolonged exposure to low temperatures may lead to the "winter disease", a metabolic disorder that significantly affects the aquaculture productions along the Northern Mediterranean coasts during winter-spring season. While sea bream susceptibility to low temperatures has been extensively investigated, the cascade of molecular events under such stressful condition is not fully elucidated.ResultsIn the present study two groups of wild sea bream were exposed for 21 days to two temperature regimes: 16 ± 0.3°C (control group) and 6.8 ± 0.3°C (cold-exposed group) and DNA microarray analysis of liver transcriptome was carried out at different time points during cold exposure.A large set of genes was found to be differentially expressed upon cold-exposure with increasingly relevant effects being observed after three weeks at low temperature. All major known responses to cold (i.e. anti-oxidant response, increased mitochondrial function, membrane compositional changes) were found to be conserved in the gilthead sea bream, while, evidence for a key role of unfolded protein response (UPR) to endoplasmic reticulum (ER) stress, during short- and long-term exposure to cold is reported here for the first time.ConclusionsTranscriptome data suggest a scenario where oxidative stress, altered lipid metabolism, ATP depletion and protein denaturation converge to induce ER stress. The resulting UPR activation further promotes conditions for cell damage, and the inability to resolve ER stress leads to severe liver dysfunction and potentially to death.Electronic supplementary materialThe online version of this article (doi:10.1186/1471-2164-15-765) contains supplementary material, which is available to authorized users.

Molecular cloning and expression analysis of scd1 gene from large yellow croaker Larimichthys crocea under cold stress

“…Severe cold weather often resulted in mass mortality of commercially important cultured species such as tilapia (Oreochromis niloticus) (Zerai et al, 2010), orange-spotted grouper (Epinephelus coioides) (Qi et al, 2013) and gilthead sea bream (Sparus aurata) (Mininni et al, 2014). It was reported that maintenance of cell membrane fluidity was an effective way to adapt to cold stress for fishes (Hsieh and Kuo, 2005;Hazel, 1979;Bell et al, 1986).…”

Fasting enhances cold resistance in fish through stimulating lipid catabolism and autophagy

“…; Mininni et al . ), and a transgenic zebrafish ( Danio rerio ) strain expressing carp muscle‐specific form III of creatine kinase showed enhanced cold resistance (Wang et al . ).…”

“…Several mechanisms related to cold adaptation in fish have been reported, including the alteration of cell-membrane fluidity (Johnston & Roots, 1964), recruitment of different muscle fibres (Gerlach et al 1990), synthesis of molecular chaperones (Fader et al 1994;Donaldson et al 2008), and generation of antifreeze proteins in freezing environments (Devries, 1971;Cao et al 2016). Moreover, several transcriptomic studies have indicated that numerous genes involved in energy metabolism are changed significantly in several fishes under cold stress (Gracey et al 2004;Mininni et al 2014), and a transgenic zebrafish (Danio rerio) strain expressing carp muscle-specific form III of creatine kinase showed enhanced cold resistance . The results of these studies suggest that energy metabolism correlates with cold resistance.…”

The Antioxidant Peroxiredoxin 6 (Prdx6) Exhibits Different Profiles in the Livers of Seawater- and Fresh Water-Acclimated Milkfish, Chanos chanos, upon Hypothermal Challenge

“…Analysis of the gilthead sea bream liver transcriptome revealed immediate and sustained activation of NFE2L2/NRF2, the main antioxidant response transcription factor, under cold stress (Mininni et al, 2014). The gene expression of antioxidant enzymes (SOD, GPx, and Cat) was also up-regulated upon acute hypothermal challenge in zebrafish livers (Wu et al, 2015).…”

“…On the other hand, changes in environmental salinities were found to be associated with the enhancement of ROS generation, whereas imbalance of the antioxidant mechanisms induced oxidative damage in aquatic organisms (Martínez-Alvarez et al, 2002; Paital and Chainy, 2010; Lushchak, 2011). Acute up-regulation of both enzymatic and non-enzymatic antioxidant mechanisms were reported in fish to neutralize ROS damage against the oxidative stress (Mininni et al, 2014; Nakano et al, 2014; Wu et al, 2015). Therefore, salinity and hypothermal stress together might enhance ROS generation and induce oxidative damage in FW low-temperature milkfish, leading to more acute up-regulation of prdx6 in the FW group (24 h) than the SW group (96 h) upon hypothermal challenge.…”