Stress response or beneficial temperature acclimation: transcriptomic signatures inAntarctic fish (Pachycara brachycephalum)

Abstract

Research on the thermal biology of Antarctic marine organisms has increased awareness of their vulnerability to climate change, as a flipside of their adaptation to life in the permanent cold and their limited capacity to acclimate to variable temperatures. Here, we employed a species-specific microarray of the Antarctic eelpout, Pachycara brachycephalum, to identify long-term shifts in gene expression after 2 months of acclimation to six temperatures between -1 and 9 °C. Changes in cellular processes comprised signalling, post-translational modification, cytoskeleton remodelling, metabolic shifts and alterations in the transcription as well as translation machinery. The magnitude of transcriptomic responses paralleled the change in whole animal performance. Optimal growth at 3 °C occurred at a minimum in gene expression changes indicative of a balanced steady state. The up-regulation of ribosomal transcripts at 5 °C and above was accompanied by the transcriptomic activation of differential protein degradation pathways, from proteasome-based degradation in the cold towards lysosomal protein degradation in the warmth. From 7 °C upwards, increasing transcript levels representing heat-shock proteins and an acute inflammatory response indicate cellular stress. Such patterns may contribute to a warm-induced energy deficit and a strong weight loss at temperatures above 6 °C. Together, cold or warm acclimation led to specific cellular rearrangements and the progressive development of functional imbalances beyond the optimum temperature. The observed temperature-specific expression profiles reveal the molecular basis of thermal plasticity and refine present understanding of the shape and positioning of the thermal performance curve of ectotherms on the temperature scale.

Transcriptomic responses to environmental temperature in eurythermal and stenothermal fishes

“…Huth and Place (2013) posit that their findings in T. bernacchii may be related to the role that HMGB1 can play in inflammation responses. Inflammation signals were also observed in heat-stressed H. antarcticus (Thorne et al, 2010) and in the Antarctic eelpout Pachycara brachycephalum (Windisch et al, 2014). Finally, many of the same genes that responded to a long-term thermal exposure also responded to an acute exposure to the same treatment temperature, albeit in the opposite direction ).…”

“…Gracey et al, 2001;Buckley et al, 2006;Buckley and Somero, 2009;Logan and Somero, 2011;Windisch et al, 2014). The magnitude and duration of heat stress, for example, both directly influence the dynamics of expression of Hsp genes Logan and Somero, 2011).…”

Transcriptome response to temperature stress in the wolf spider Pardosa pseudoannulata (Araneae: Lycosidae)

“…High mitochondrial densities have been found in other cold‐acclimated poikilotherm species such as fish (Clarke and Johnston 1999; Windisch et al. 2014), with a positive impact demonstrated wherein mitochondrial ribosomal proteins displayed high transcription rates at low temperatures (Windisch et al. 2014).…”

“…2014), with a positive impact demonstrated wherein mitochondrial ribosomal proteins displayed high transcription rates at low temperatures (Windisch et al. 2014). The protein synthesis machinery is one of the largest multienzyme complexes in cells and, ribosome formation and its functioning were concerned with the majority of universal proteins (Korobeinikova et al.…”

“…The magnitude of transcriptome response should be consistent with the change in whole animal performance, and it might be conjectured that spiders should exhibit minimal gene expression changes taking their optimal 25°C subsistence temperature as a balanced steady state (Windisch et al. 2014). In contrast, physiological response to thermal stress is manifold and complex, and many genes, proteins, metabolic pathways have been shown to be involved in this process in animals (Goto 2001; Overgaard et al.…”