Temperature-dependent protein synthesis capacities in Antarctic and temperate (North Sea) fish (Zoarcidae)

Storch, Daniela; Lannig, Gisela; Pörtner, Hans‐Otto

doi:10.1242/jeb.01632

Cited by 39 publications

(37 citation statements)

References 51 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…2 A), most notably in the coelevation of 29 ribosomal protein genes (Table S3 in SI Appendix). The increase in ribosomal biogenesis suggests enhanced protein synthesis capacity in this tissue, which was reported for the gill and white muscle of another cold-adapted Antarctic teleost, the zoarcid Pachycara brachycephalum (21).…”

Section: Resultssupporting

confidence: 66%

Transcriptomic and genomic evolution under constant cold in Antarctic notothenioid fish

Chen

Cheng

Zhang

et al. 2008

Proc. Natl. Acad. Sci. U.S.A.

232

215

View full text Add to dashboard Cite

The antifreeze glycoprotein-fortified Antarctic notothenioid fishes comprise the predominant fish suborder in the isolated frigid Southern Ocean. Their ecological success undoubtedly entailed evolutionary acquisition of a full suite of cold-stable functions besides antifreeze protection. Prior studies of adaptive changes in these teleost fishes generally examined a single genotype or phenotype. We report here the genome-wide investigations of transcriptional and genomic changes associated with Antarctic notothenioid cold adaptation. We sequenced and characterized 33,560 ESTs from four tissues of the Antarctic notothenioid Dissostichus mawsoni and derived 3,114 nonredundant protein gene families and their expression profiles. Through comparative analyses of same-tissue transcriptome profiles of D. mawsoni and temperate/tropical teleost fishes, we identified 177 notothenioid protein families that were expressed many fold over the latter, indicating cold-related up-regulation. These up-regulated gene families operate in protein biosynthesis, protein folding and degradation, lipid metabolism, antioxidation, antiapoptosis, innate immunity, choriongenesis, and others, all of recognizable functional importance in mitigating stresses in freezing temperatures during notothenioid life histories. We further examined the genomic and evolutionary bases for this expressional up-regulation by comparative genomic hybridization of DNA from four pairs of Antarctic and basal non-Antarctic notothenioids to 10,700 D. mawsoni cDNA probes and discovered significant to astounding (3-to >300-fold, P < 0.05) Antarctic-specific duplications of 118 protein-coding genes, many of which correspond to the up-regulated gene families. Results of our integrative tripartite study strongly suggest that evolution under constant cold has resulted in dramatic genomic expansions of specific protein gene families, augmenting gene expression and gene functions contributing to physiological fitness of Antarctic notothenioids in freezing polar conditions. cold adaptation ͉ comparative genomics ͉ gene duplication ͉ genome evolution ͉ retrotransposon

show abstract

Section: Resultssupporting

confidence: 66%

Transcriptomic and genomic evolution under constant cold in Antarctic notothenioid fish

Chen

Cheng

Zhang

et al. 2008

Proc. Natl. Acad. Sci. U.S.A.

232

215

View full text Add to dashboard Cite

show abstract

“…3), cycloheximide sensitive respiration was found to be significantly higher in most of the highAntarctic nototheniids than in the sub-Antarctic species, while ouabain sensitive respiration displayed a contrasting trend and was somewhat lower. In the context with earlier observations by other authors, the observed bias in energy allocation may indicate that the stenothermal high Antarctic nototheniids possess greater protein synthesis capacities than the more eurythermal species but lower capacities of active ion regulation: Storch et al (2005) observed higher protein synthesis capacities in the cold-eurythermal Antarctic eelpout P. brachycephalum as compared to the warm-eurythermal common eelpout Zoarces viviparus, and other authors also found evidence for cold compensated protein synthesis in high-Antarctic fish (Smith and Haschemeyer 1980) and sea urchin embryos (Marsh et al 2001). Furthermore, several studies investigating pH and ion regulation in eurythermal and stenothermal fish (Po¨rtner and Sartoris 1999;Bock et al 2001;Sartoris et al 2003a) found the greater part of pH regulation in eurythermal fish to be dependent on active processes like regulation via Na + /K + -ATPase, while in stenothermal fish, less costly passive processes prevailed.…”

Section: Variability In Energy Budgetssupporting

confidence: 51%

Thermal sensitivity of cellular energy budgets in some Antarctic fish hepatocytes

2005

View full text Add to dashboard Cite

Oxygen demand elicited by the main cellular energy consumers was examined in isolated hepatocytes of sub-Antarctic (Lepidonotothen larseni) and highAntarctic notothenioids (Trematomus eulepidotus, Trematomus pennellii, Trematomus lepidorhinus, Trematomus bernacchii, Artedidraco orianae) and in a zoarcid (Pachycara brachycephalum) fish with respect to the role of cellular metabolism in co-defining thermal tolerance. The relative proportions of energy allocated to protein and RNA/DNA synthesis, ion regulation and ATP synthesis were quantified between 0°C and 15°C by analysis of inhibitor sensitive cellular respiration. In all the investigated species, protein synthesis constituted 25-37%, RNA synthesis 24-35%, Na + /K + -ATPase 40-45% and mitochondrial ATP synthesis 57-65% of total respiration. The sub-Antarctic nototheniid L. larseni displayed lower cellular protein synthesis rates but somewhat higher active ion regulation activities than its high-Antarctic confamilials, as is typical for more eurythermal species. Assumed thermal optima were mirrored in minimized overall cellular energy demand. In the sub-Antarctic L. larseni and P. brachycephalum, minima of oxygen consumption were located between 3°C and 6°C, indicating elevated energy turnover below and above these temperatures. In contrast, the highAntarctic species displayed progressively rising respiration rates during warming with a cellular energetic minimum at 0°C. The sub-Antarctic nototheniid and the zoarcid showed signs of cold-eurythermy and appear to live close to their lower limit of thermal tolerance, while high-Antarctic notothenioids show high degrees of energetic efficiency at 0°C. All cellular preparations maintained energy budgets over a wide thermal range, supporting the recent concept that thermal limits are set by oxygen and associated energy limitations at the whole organism level.

show abstract

“…Indeed, the high RNA/ protein ratio for APEH-2 Tb may represent a possible approach to maintain the capability for an immediate response to the oxidative environment when the levels of damaged proteins become too high. Recently, it has been reported that the Antarctic invertebrates maintain elevated RNA/protein ratios, through increased RNA levels to counterbalance the low RNA translational efficiency at low temperatures; a different strategy has been seen for the Antarctic eelpout (Pachycara brachycephalum), which shows improved RNA translational capacity [42]. However, further studies will be required to determine whether the strategies adopted by Antarctic fish to counteract the lower protein synthesis rates involve an increase in RNA concentration, an enhancement of translational capacity, or a combination of both mechanisms.…”

Section: Discussionmentioning

confidence: 99%

A novel class of bifunctional acylpeptide hydrolases – potential role in the antioxidant defense systems of the Antarctic fish Trematomus bernacchii

et al. 2013

View full text Add to dashboard Cite

Oxidative challenge is an important factor affecting the adaptive strategies of Antarctic fish, but data on antioxidant defenses in these organisms remain scarce. In this context, a key role could be played by acylpeptide hydrolase (APEH), which was recently hypothesized to participate in the degradation of oxidized and cytotoxic proteins, although its physiological function is still not fully clarified. This study represents the first report on piscine members of this enzyme family, specifically from the Antarctic teleost Trematomus bernacchii. The cDNAs corresponding to two apeh genes were isolated, and the respective proteins were functionally and structurally characterized with the aim of understanding the biological significance of these proteases in Antarctic fish. Both APEH isoforms (APEH-1 Tb and APEH-2 Tb ) showed distinct temperature-kinetic behavior, with significant differences in the K m values. Moreover, beside the typical acylpeptide hydrolase activity, APEH-2 Tb showed remarkable oxidized protein endohydrolase activity towards oxidized BSA, suggesting that this isoform could play a homeostatic role in removing oxidatively damaged proteins, sustaining the antioxidant defense systems. The 3D structures of both APEHs were predicted, and a possible relationship was found between the substrate specificity/affinity and the marked changes in the number of charged residues and hydrophobicity properties surrounding their catalytic sites. Our results demonstrated the occurrence of two APEH isoforms in T. bernacchii, belonging to different phylogenetic clusters, identified for the first time, and showing distinct molecular and temperature-kinetic behaviors. In addition, we suggest that the members of the new cluster 'APEH-2' could participate in reactive oxygen species detoxification as phase 3 antioxidant enzymes, enhancing the protein degradation machinery.

show abstract

Temperature-dependent protein synthesis capacities in Antarctic and temperate (North Sea) fish (Zoarcidae)

Cited by 39 publications

References 51 publications

Transcriptomic and genomic evolution under constant cold in Antarctic notothenioid fish

Transcriptomic and genomic evolution under constant cold in Antarctic notothenioid fish

Thermal sensitivity of cellular energy budgets in some Antarctic fish hepatocytes

A novel class of bifunctional acylpeptide hydrolases – potential role in the antioxidant defense systems of the Antarctic fish Trematomus bernacchii

Contact Info

Product

Resources

About