Thermal sensitivity of cell metabolism of different Antarctic fish species mirrors organism temperature tolerance

Despite cold adaptation, Antarctic fish show lower growth than expected from the van’t Hoff’s Q10 rule. Protein synthesis is one of the main energy-consuming processes, which is downregulated under energy deficiency. Considering the effect of temperature on growth performance, we tested if temperature-dependent cellular energy allocation to protein synthesis correlates with temperature-dependent whole-animal growth and thus thermal tolerance. Cell respiration and energy expenditure for protein synthesis were determined in hepatocytes of the circumpolar-distributed Antarctic eelpout Pachycara brachycephalum after warm acclimation (0 °C vs 5 °C) and, of two notothenioids the sub-Antarctic Lepidonotothen squamifrons and the high-Antarctic icefish Chionodraco hamatus. We used intermittent-flow respirometry to analyse cellular response to acute warming from 5 to 10 °C (P. brachycephalum) and from 1 to 5 °C (L. squamifrons, C. hamatus). Warming-induced rise in respiration was similar between 0- and 5 °C-acclimated P. brachycephalum and between L. squamifrons and C. hamatus. Irrespective of acclimation, warming decreased energy expenditure for protein synthesis in P. brachycephalum, which corresponds to reduced whole-animal growth at temperatures > 5 °C. Warming doubled energy expenditure for protein synthesis in L. squamifrons but had no effect on C. hamatus indicating that L. squamifrons might benefit from warmer waters. The species-specific temperature effect on energy expenditure for protein synthesis is discussed to mirror thermal sensitivity of whole-animal growth performance, thereby paralleling the degree of cold adaptation. Clearly more data are necessary including measurements at narrower temperature steps particularly for C. hamatus and an increased species’ number per ecotype to reinforce presented link between cellular and whole-animal thermal sensitivity

Temperature but not ocean acidification affects energy metabolism and enzyme activities in the blue mussel, Mytilus edulis

1. In mosaic marine habitats, such as intertidal zones, ocean acidification (OA) is exacerbated by high variability of pH, temperature, and biological CO2 production. The nonlinear interactions among these drivers can be context-specific and their effect on organisms in these habitats remains largely unknown, warranting further investigation. 2. We were particularly interested in Mytilus edulis (the blue mussel) from intertidal zones of the Gulf of Maine (GOM), USA, for this study. GOM is a hot spot of global climate change (average sea surface temperature (SST) increasing by \u3e0.2°C/year) with \u3e60% decline in mussel population over the past 40 years. 3. Here, we utilize bioenergetic underpinnings to identify limits of stress tolerance in M. edulis from GOM exposed to warming and OA. We have measured whole organism oxygen consumption rates and metabolic biomarkers in mussels exposed to control and elevated temperatures (10 vs. 15°C, respectively) and current and moderately elevated PCO2 levels (~400 vs. 800 µatm, respectively). 4. Our study demonstrates that adult M. edulis from GOM are metabolically resilient to the moderate OA scenario but responsive to warming as seen in changes in metabolic rate, energy reserves (total lipids), metabolite profiles (glucose and osmolyte dimethyl amine), and enzyme activities (carbonic anhydrase and calcium ATPase). 5. Our results are in agreement with recent literature that OA scenarios for the next 100–300 years do not affect this species, possibly as a consequence of maintaining its in vivo acid-base balance

Impact of Ocean Acidification on Energy Metabolism of Oyster, Crassostrea gigas—Changes in Metabolic Pathways and Thermal Response

Climate change with increasing temperature and ocean acidification (OA) poses risks for marine ecosystems. According to Pörtner and Farrell [1], synergistic effects of elevated temperature and CO2-induced OA on energy metabolism will narrow the thermal tolerance window of marine ectothermal animals. To test this hypothesis, we investigated the effect of an acute temperature rise on energy metabolism of the oyster, Crassostrea gigas chronically exposed to elevated CO2 levels (partial pressure of CO2 in the seawater ~0.15 kPa, seawater pH ~ 7.7). Within one month of incubation at elevated Pco2 and 15 °C hemolymph pH fell (pHe = 7.1 ± 0.2 (CO2-group) vs. 7.6 ± 0.1 (control)) and Peco2 values in hemolymph increased (0.5 ± 0.2 kPa (CO2-group) vs. 0.2 ± 0.04 kPa (control)). Slightly but significantly elevated bicarbonate concentrations in the hemolymph of CO2-incubated oysters ([HCO− 3]e = 1.8 ± 0.3 mM (CO2-group) vs. 1.3 ± 0.1 mM (control)) indicate only minimal regulation of extracellular acid-base status. At the acclimation temperature of 15 °C the OA-induced decrease in pHe did not lead to metabolic depression in oysters as standard metabolism rates (SMR) of CO2-exposed oysters were similar to controls. Upon acute warming SMR rose in both groups, but displayed a stronger increase in the CO2-incubated group. Investigation in isolated gill cells revealed a similar temperaturedependence of respiration between groups. Furthermore, the fraction of cellular energy demand for ion regulation via Na+/K+-ATPase was not affected by chronic hypercapnia or temperature. Metabolic profiling using 1H-NMR spectroscopy revealed substantial changes in some tissues following OA exposure at 15 °C. In mantle tissue alanine and ATP levels decreased significantly whereas an increase in succinate levels was observed in gill tissue. These findings suggest shifts in metabolic pathways following OA-exposure. Our study confirms that OA affects energy metabolism in oysters and suggests that climate change may affect populations of sessile coastal invertebrates such as mollusks

Impact of ocean acidification on escape performance of the king scallop, Pecten maximus, from Norway

The ongoing process of ocean acidification already affects marine life, and according to the concept of oxygen and capacity limitation of thermal tolerance, these effects may be intensified at the borders of the thermal tolerance window. We studied the effects of elevated CO2 concentrations on clapping performance and energy metabolism of the commercially important scallop Pecten maximus. Individuals were exposed for at least 30 days to 4 °C (winter) or to 10 °C (spring/summer) at either ambient (0.04 kPa, normocapnia) or predicted future PCO2 levels (0.11 kPa, hypercapnia). Cold-exposed (4 °C) groups revealed thermal stress exacerbated by PCO2 indicated by a high mortality overall and its increase from 55 % under normocapnia to 90 % under hypercapnia. We therefore excluded the 4 °C groups from further experimentation. Scallops at 10 °C showed impaired clapping performance following hypercapnic exposure. Force production was significantly reduced although the number of claps was unchanged between normocapnia- and hypercapnia-exposed scallops. The difference between maximal and resting metabolic rate (aerobic scope) of the hypercapnic scallops was significantly reduced compared with normocapnic animals, indicating a reduction in net aerobic scope. Our data confirm that ocean acidification narrows the thermal tolerance range of scallops resulting in elevated vulnerability to temperature extremes and impairs the animal’s performance capacity with potentially detrimental consequences for its fitness and survival in the ocean of tomorrow

Naturally acidified habitat selects for ocean acidification–tolerant mussels

Ocean acidification severely affects bivalves, especially their larval stages. Consequently, the fate of this ecologically and economically important group depends on the capacity and rate of evolutionary adaptation to altered ocean carbonate chemistry. We document successful settlement of wild mussel larvae (Mytilus edulis) in a periodically CO2-enriched habitat. The larval fitness of the population originating from the CO2-enriched habitat was compared to the response of a population from a nonenriched habitat in a common garden experiment. The high CO2–adapted population showed higher fitness under elevated Pco2 (partial pressure of CO2) than the non-adapted cohort, demonstrating, for the first time, an evolutionary response of a natural mussel population to ocean acidification. To assess the rate of adaptation, we performed a selection experiment over three generations. CO2 tolerance differed substantially between the families within the F1 generation, and survival was drastically decreased in the highest, yet realistic, Pco2 treatment. Selection of CO2-tolerant F1 animals resulted in higher calcification performance of F2 larvae during early shell formation but did not improve overall survival. Our results thus reveal significant short-term selective responses of traits directly affected by ocean acidification and long-term adaptation potential in a key bivalve species. Because immediate response to selection did not directly translate into increased fitness, multigenerational studies need to take into consideration the multivariate nature of selection acting in natural habitats. Combinations of short-term selection with long-term adaptation in populations from CO2-enriched versus nonenriched natural habitats represent promising approaches for estimating adaptive potential of organisms facing global change

In vivo 31P-MRS of muscle bioenergetics in marine invertebrates: Future ocean limits scallops' performance

Object: Dynamic in vivo 31P-NMR spectroscopy in combination with Magnetic Resonance Imaging (MRI) was used to study muscle bioenergetics of boreal and Arctic scallops (Pecten maximus and Chlamys islandica) to test the hypothesis that future Ocean Warming and Acidification (OWA) will impair the performance of marine invertebrates. Materials & methods: Experiments were conducted following the recommendations for studies of muscle bioenergetics in vertebrates. Animals were long-term incubated under different environmental conditions: controls at 0 °C for C. islandica and 15 °C for P. maximus under ambient PCO2 of 0.039 kPa, a warm exposure with +5 °C (5 °C and 20 °C, respectively) under ambient PCO2 (OW group), and a combined exposure to warmed acidified conditions (5 °C and 20 °C, 0.112 kPa PCO2, OWA group). Scallops were placed in a 4.7 T MR animal scanner and the energetic status of the adductor muscle was determined under resting conditions using in vivo 31P-NMR spectroscopy. The surplus oxidative flux (Qmax) was quantified by recording the recovery of arginine phosphate (PLA) directly after moderate swimming exercise of the scallops. Results: Measurements led to reproducible results within each experimental group. Under projected future conditions resting PLA levels (PLArest) were reduced, indicating reduced energy reserves in warming exposed scallops per se. In comparison to vertebrate muscle tissue surplus Qmax of scallop muscle was about one order of magnitude lower. This can be explained by lower mitochondrial contents and capacities in invertebrate than vertebrate muscle tissue. Warm exposed scallops showed a slower recovery rate of PLA levels (kPLA) and a reduced surplus Qmax. Elevated PCO2 did not affected PLA recovery further. Conclusion: Dynamic in vivo 31P-NMR spectroscopy revealed constrained residual aerobic power budgets in boreal and Arctic scallops under projected ocean warming and acidification indicating that scallops are susceptible to future climate change. The observed reduction in muscular PLArest of scallops coping with a warmer and acidified ocean may be linked to an enhanced energy demand and reduced oxygen partial pressures (PO2) in their body fluids. Delayed recovery from moderate swimming at elevated temperature is a result of reduced PLArest concentrations associated with a warm-induced reduction of a residual aerobic power budget

Sustainable fish feeds: potential of emerging protein sources in diets for juvenile turbot (Scophthalmus maximus) in RAS

In Europe, turbot aquaculture has a high potential for sustainable production, but the low tolerance to fishmeal replacement in the diet represents a big issue. Therefore, this study investigated the effects of more sustainable feed formulations on growth and feed performance, as well as nutritional status of juvenile turbot in recirculating aquaculture systems. In a 16-week feeding trial with 20 g juvenile turbot, one control diet containing traditional fishmeal, fish oil and soy products and two experimental diets where 20% of the fishmeal was replaced either with processed animal proteins (PAP) or with terrestrial plant proteins (PLANT) were tested. Irrespective of diets, growth performance was similar between groups, whereas the feed performance was significantly reduced in fish of the PAP group compared to the control. Comparing growth, feed utilisation and biochemical parameters, the results indicate that the fish fed on PAP diet had the lowest performance. Fish fed the PLANT diet had similar feed utilisation compared to the control, whereas parameters of the nutritional status, such as condition factor, hepato-somatic index and glycogen content showed reduced levels after 16 weeks. These effects in biochemical parameters are within the physiological range and therefore not the cause of negative performance. Since growth was unaffected, the lower feed performance of fish that were fed the PAP formulation might be balanced by the cost efficient formulation in comparison to the commercial and the PLANT formulations. Present study highlights the suitability of alternative food formulation for farmed fish

Heat hardening enhances metabolite-driven thermoprotection in the Mediterranean mussel Mytilus galloprovincialis

Introduction: Temperature affects organisms’ metabolism and ecological performance. Owing to climate change, sea warming constituting a severe source of environmental stress for marine organisms, since it increases at alarming rates. Rapid warming can exceed resilience of marine organisms leading to fitness loss and mortality. However, organisms can improve their thermal tolerance when briefly exposed to sublethal thermal stress (heat hardening), thus generating heat tolerant phenotypes.Methods: We investigated the “stress memory” effect caused by heat hardening on M. galloprovincialis metabolite profile of in order to identify the underlying biochemical mechanisms, which enhance mussels’ thermal tolerance.Results: The heat hardening led to accumulation of amino acids (e.g., leucine, isoleucine and valine), including osmolytes and cytoprotective agents with antioxidant and anti-inflammatory properties that can contribute to thermal protection of the mussels. Moreover, proteolysis was inhibited and protein turnover regulated by the heat hardening. Heat stress alters the metabolic profile of heat stressed mussels, benefiting the heat-hardened individuals in increasing their heat tolerance compared to the non-heat-hardened ones.Discussion: These findings provide new insights in the metabolic mechanisms that may reinforce mussels’ tolerance against thermal stress providing both natural protection and potential manipulative tools (e.g., in aquaculture) against the devastating climate change effects on marine organisms

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

SummaryFor an evaluation of effects of seasonal cold acclimation and evolutionary cold adaptation on protein synthesis capacity the protein synthesis apparatus was isolated from the gills and white muscle of Antarctic eelpout Pachycara brachycephalum and North Sea eelpout Zoarces viviparus. Both species had been acclimated to 0 (control) and 5°C (Antarctic) and 5 and 10°C (North Sea control), respectively. The translational capacities of the protein synthesis machineries were determined in an optimised cell free in vitro system. The results demonstrate that tissues from the polar zoarcid possess cold adapted protein synthesis machineries indicated by low activation energies, and, especially, high RNA translational capacities at similar RNA:protein ratios when compared to temperate zoarcids at 10°C. When both species were brought to 5°C, the temperate species displayed cold compensated protein synthesis capacities caused by elevated RNA:protein ratios. Warm exposure (from 0 to 5°C) of the Antarctic zoarcid revealed a capacity for thermal acclimation indicated by a reduction in protein synthesis capacities associated with lower RNA:protein ratios