Thermal acclimation in Antarctic fish: transcriptomic profiling of metabolic pathways

SUMMARYIn the eurythermal cuttlefish Sepia officinalis, performance depends on hearts that ensure systemic oxygen supply over a broad range of temperatures. We therefore aimed to identify adjustments in energetic cardiac capacity and underlying mitochondrial function supporting thermal acclimation and adaptation that could be crucial for the cuttlefishʼs competitive success in variable environments. Two genetically distinct cuttlefish populations were acclimated to 11, 16 and 21°C. Subsequently, skinned and permeabilised heart fibres were used to assess mitochondrial functioning by means of high-resolution respirometry and a substrate-inhibitor protocol, followed by measurements of cardiac citrate synthase and cytosolic enzyme activities. Temperate English Channel cuttlefish had lower mitochondrial capacities but larger hearts than subtropical Adriatic cuttlefish. Warm acclimation to 21°C decreased mitochondrial complex I activity in Adriatic cuttlefish and increased complex IV activity in English Channel cuttlefish. However, compensation of mitochondrial capacities did not occur during cold acclimation to 11°C. In systemic hearts, the thermal sensitivity of mitochondrial substrate oxidation was high for proline and pyruvate but low for succinate. Oxygen efficiency of catabolism rose as temperature changed from 11 to 21°C via shifts to oxygen-conserving oxidation of proline and pyruvate and via reduced relative proton leak. The changes observed for substrate oxidation, mitochondrial complexes, relative proton leak and heart mass improve energetic efficiency and essentially seem to extend tolerance to high temperatures and reduce associated tissue hypoxia. We conclude that cuttlefish sustain cardiac performance and, thus, systemic oxygen delivery over short-and long-term changes of temperature and environmental conditions by multiple adjustments in cellular and mitochondrial energetics. Supplementary material available online at

Section: Mitochondrial Complexesmentioning

confidence: 99%

Mitochondrial dynamics underlying thermal plasticity of cuttlefish (Sepia officinalis) hearts

Oellermann

Pörtner

Mark

2012

“…This example is interesting given that notothenioids maintain a serum osmolality nearly double that of temperate fishes and only upon warm acclimation do their serum levels resemble those of warmer water species. In other illustrations, warm-acclimated T. bernacchii displayed significant changes in CS and LDH activities in heart and skeletal muscle , while P. borchgrevinki showed an increase in LDH and cytochrome c oxidase activity in skeletal muscle, possibly attributable to an increase in metabolic activity that reflects higher energetic costs associated with living at warmer temperatures (Windisch et al, 2011). A decrease in lipid metabolic capacity with warm acclimation was detected in T. bernacchii and Pachycara brachycephalum (Windisch et al, 2011), suggesting a potential shift towards carbohydrates as the primary source of metabolic fuel at higher temperatures.…”

Section: Acclimation Capacitymentioning

confidence: 93%

“…In other illustrations, warm-acclimated T. bernacchii displayed significant changes in CS and LDH activities in heart and skeletal muscle , while P. borchgrevinki showed an increase in LDH and cytochrome c oxidase activity in skeletal muscle, possibly attributable to an increase in metabolic activity that reflects higher energetic costs associated with living at warmer temperatures (Windisch et al, 2011). A decrease in lipid metabolic capacity with warm acclimation was detected in T. bernacchii and Pachycara brachycephalum (Windisch et al, 2011), suggesting a potential shift towards carbohydrates as the primary source of metabolic fuel at higher temperatures. This shift is possibly to support carbohydrate-based anaerobic metabolism that may occur under increased hypoxemic conditions or, alternatively, it is possible that the reduction in ATP-generation potential, particularly in T. bernacchii, is a consequence of compromised functions at warmer temperatures.…”

Section: Acclimation Capacitymentioning

confidence: 93%

Antarctic notothenioid fish: what are the future consequences of ‘losses’ and ‘gains’ acquired during long-term evolution at cold and stable temperatures?

Beers

Jayasundara

2015

Antarctic notothenioids dominate the fish fauna of the Southern Ocean. Evolution for millions of years at cold and stable temperatures has led to the acquisition of numerous biochemical traits that allow these fishes to thrive in sub-zero waters. The gain of antifreeze glycoproteins has afforded notothenioids the ability to avert freezing and survive at temperatures often hovering near the freezing point of seawater. Additionally, possession of cold-adapted proteins and membranes permits them to sustain appropriate metabolic rates at exceptionally low body temperatures. The notothenioid genome is also distinguished by the disappearance of traits in some species, losses that might prove costly in a warmer environment. Perhaps the best-illustrated example is the lack of expression of hemoglobin in white-blooded icefishes from the family Channichthyidae. Loss of key elements of the cellular stress response, notably the heat shock response, has also been observed. Along with their attainment of cold tolerance, notothenioids have developed an extreme stenothermy and many species perish at temperatures only a few degrees above their habitat temperatures. Thus, in light of today's rapidly changing climate, it is critical to evaluate how these extreme stenotherms will respond to rising ocean temperatures. It is conceivable that the remarkable cold specialization of notothenioids may ultimately leave them vulnerable to future thermal increases and threaten their fitness and survival. Within this context, our review provides a current summary of the biochemical losses and gains that are known for notothenioids and examines these cold-adapted traits with a focus on processes underlying thermal tolerance and acclimation capacity.

“…Animals of small size classes were not suitable for tissue sampling. Enzyme extracts were prepared following the protocol by Windisch et al (2011). In brief, frozen samples were homogenized in 10 volumes of buffer (20 mmol l −1 Tris-HCl, 1 mmol l −1 EDTA, 0.1% Triton X-100, pH 7.5), either directly with a glass homogenizer (small samples) or by grinding the tissue under liquid nitrogen first followed by mixing of the powdered tissue with the adequate buffer volume by use of a vortex.…”

Section: Enzyme Activitiesmentioning

confidence: 99%

Does the membrane pacemaker theory of metabolism explain the size dependence of metabolic rate in marine mussels?

Сухотин

Fokina

Руоколайнен

et al. 2017

Self Cite

According to the membrane pacemaker theory of metabolism (MPT), allometric scaling of metabolic rate in animals is determined by the composition of cellular and mitochondrial membranes, which changes with body size in a predictable manner. MPT has been elaborated from interspecific comparisons in mammals. It projects that the degree of unsaturation of membrane phospholipids decreases in larger organisms, thereby lowering ion permeability of the membranes and making cellular, and thus whole-animal metabolism more efficient. Here, we tested the applicability of the MPT to a marine ectotherm, the mussel Mytilus edulis at the intraspecific level. We determined effects of body mass on wholeorganism, tissue and cellular oxygen consumption rates, on heart rate, metabolic enzyme activities and on the lipid composition of membranes. In line with allometric patterns, the organismal functions and processes such as heart rate, whole-animal respiration rate and phospholipid contents showed a mass-dependent decline. However, the allometry of tissue and cellular respiration and activity of metabolic enzymes was poor; fatty acid unsaturation of membrane phospholipids of gill tissue was independent of animal size. It is thus conceivable that most of the metabolic allometry observed at the organismal level is determined by systemic functions. These wholeorganism patterns may be supported by energy savings associated with growing cell size but not by structural changes in membranes. Overall, the set of processes contributing to metabolic allometry in ectotherms may differ from that operative in mammals and birds, with a reduced involvement of the mechanisms proposed by the MPT.