Physiological adaptations to high intertidal life involve improved water conservation abilities and metabolic rate depression in Littorina saxatilis

132

114

SUMMARYContemporary theory for thermal adaptation of ectothermic metazoans focuses on the maximization of energy gain and performance (locomotion and foraging). Little consideration is given to the selection for mechanisms that minimize resting energy loss in organisms whose energy gain is severely constrained. We tested a hypothetical framework for thermal performance of locomotor activity (a proxy for energy gain) and resting metabolism (a proxy for energy loss) in energetically compromised snails in the littoral fringe zone, comparing this with existing theory. In contrast to theory, the thermal ranges and optima for locomotor performance and metabolic performance of Echinolittorina malaccana are mismatched, and energy gain is only possible at relatively cool temperatures. To overcome thermal and temporal constraints on energy gain while experiencing high body temperatures (23-50°C), these snails depress resting metabolism between 35 and 46°C (thermally insensitive zone). The resulting bimodal relationship for metabolism against temperature contrasts with the unimodal or exponential relationships of most ectotherms. Elevation of metabolism above the breakpoint temperature for thermal insensitivity (46°C) coincides with the induction of a heat shock response, and has implications for energy expenditure and natural selection. Time-dependent mortality is initiated at this breakpoint temperature, suggesting a threshold above which the rate of energy demand exceeds the capacity for cellular energy generation (rate of ATP turnover). Mortality in a thermal range that elevates rather than limits aerobic metabolism contrasts with the hypothesis that cellular oxygen deficiency underlies temperature-related mortality. The findings of this study point to the need to incorporate aspects of resting metabolism and energy conservation into theories of thermal adaptation.

Section: Introductionmentioning

confidence: 54%

Section: Metabolic Performancementioning

confidence: 99%

Thermal adaptation in the intertidal snailEchinolittorina malaccanacontradicts current theory by revealing the crucial roles of resting metabolism

Marshall

Dong

McQuaid

et al. 2011

132

114

“…However, ambient oxygen levels in air are approximately 30 times higher than in seawater, implying higher oxygen availability and lower costs of ventilation in air-breathing animals. During prolonged air exposure at 30°C, more than 98% of total (aerobic and anaerobic) ATP turnover in L. saxatilis was supplied by aerobic pathways (Sokolova and Pörtner, 2001a). Moreover, succinate accumulation, which indicates mitochondrial anaerobiosis, was very low, and the main anaerobic end product in air was alanine (Sokolova and Pörtner, 2001a), suggesting that mitochondria remained predominantly aerobic, and anaerobic metabolism was mostly restricted to the cytosolic compartment (Grieshaber et al, 1994).…”

Section: Heat-induced Loss Of Aerobic Scopementioning

confidence: 91%

“…During prolonged air exposure at 30°C, more than 98% of total (aerobic and anaerobic) ATP turnover in L. saxatilis was supplied by aerobic pathways (Sokolova and Pörtner, 2001a). Moreover, succinate accumulation, which indicates mitochondrial anaerobiosis, was very low, and the main anaerobic end product in air was alanine (Sokolova and Pörtner, 2001a), suggesting that mitochondria remained predominantly aerobic, and anaerobic metabolism was mostly restricted to the cytosolic compartment (Grieshaber et al, 1994). Succinate accumulation contributed only 5-12% to anaerobic ATP turnover during air exposure at high temperatures in L. saxatilis, the rest being supplied by alanine accumulation and depletion of high-energy phosphates.…”

Section: Heat-induced Loss Of Aerobic Scopementioning

confidence: 99%

Metabolic plasticity and critical temperatures for aerobic scope in a eurythermal marine invertebrate (Littorina saxatilis, Gastropoda: Littorinidae) from different latitudes

Sokolova

Pörtner

2003

200

107

SUMMARYEffects of latitudinal cold adaptation and cold acclimation on metabolic rates and aerobic scope were studied in the eurythermal marine gastropod Littorina saxatilis from temperate North Sea and sub-arctic White Sea areas. Animals were acclimated for 6-8 weeks at control temperature (13°C) or at 4°C, and their respiration rates were measured during acute temperature change (1-1.5°C h-1) in a range between 0°C and 32°C. In parallel, the accumulation of anaerobic end products and changes in energy status were monitored. Starting from 0°C, aerobic metabolic rates of L. saxatilis rose quickly with increasing temperatures up to a point at or slightly above the respective acclimation temperature. Beyond this value, thermal sensitivity of oxygen consumption rate (V̇O2) greatly decreased in a wide, 15°C range of experimental temperatures. This change in metabolic regulation was also reflected in the activation energy of aerobic metabolism (Ea), which was approximately seven times lower at temperatures above Arrhenius breakpoint temperatures (ABTs) than at temperatures below ABTs. Warming progressively led to a discrepancy between energy demand and energy production, as demonstrated by a decrease in the levels of high-energy phosphates [phosho-L-arginine (PLA) and ATP], and resulted in the onset of anaerobiosis at critically high temperatures, indicating a limitation of aerobic scope. The comparison of aerobic and anaerobic metabolic rates in L. saxatilis in air and water suggests that the heat-induced onset of anaerobiosis is due to the insufficient oxygen supply to tissues at high temperatures. Cold acclimation led to an increase in aerobic metabolic rates and a considerable downward shift of the upper critical temperature in North Sea L. saxatilis but not in White Sea L. saxatilis. Limited metabolic plasticity in response to cold acclimation in sub-arctic White Sea snails as compared with their temperate North Sea counterparts suggests that metabolic depression occurs during overwintering under the more extreme winter conditions at the White Sea.

“…A characteristic feature of the cellular physiology of intertidal mollusks, including oysters, is their capability for metabolic rate depression under conditions of environmental stress (Hochachka and Guppy, 1987;Hand and Hardewig, 1996;Storey, 1988). It has been shown that a variety of stressors, particularly those that affect ATP production such as hypoxia/anoxia, subfreezing and freezing temperatures, severe osmotic stress, result in a drastic downregulation of the use of ATP to 5-20% of the normal levels in marine mollusks (Storey and Storey, 1990;Storey and Churchill, 1995;Sokolova et al, 2000;Sokolova and Pörtner, 2001). This stress-induced decrease in ATP turnover and cellular energy demand may be important in allowing some crucial energy-dependent processes (e.g.…”

Section: Cadmium-induced Apoptosis In Oyster Hemocytesmentioning

confidence: 99%

Cadmium-induced apoptosis in oyster hemocytes involves disturbance of cellular energy balance but no mitochondrial permeability transition

Sokolova

Evans

Hughes

2004

190

111

SUMMARY Exposure to environmentally prevalent heavy metals such as cadmium can have detrimental effects on a variety of commercially and ecologically important species such as oysters. Since Cd2+ is known to induce apoptosis in immune cells of vertebrates, we have investigated the effects of this metal on isolated oyster hemocytes, the main cellular immune defense in mollusks. Enhanced apoptosis of these cells could conceivably create immunosuppressed conditions in these organisms and result in reduced disease resistance and increased opportunistic infection, resulting in decline of their populations. Cd2+ exposure induced apoptosis in oyster hemocytes in a dose-dependent manner in the range of 10-100 μmol l-1, as indicated by the translocation of phosphatidylserine to the outer leaflet of the plasma membrane. At higher concentrations (200-1000 μmol l-1), there was no further increase in apoptosis but a significant increase in the level of necrosis. In stark contrast to vertebrate immune cells, there was no decrease in the mitochondrial membrane potential or activation of caspases in response to Cd2+ in the apoptotic range. Surprisingly, Cd2+ exposure in this range did cause a significant decrease in intracellular ATP levels, indicating a severe disturbance of energy metabolism. Similarly, Cd2+ exposure of isolated mitochondria resulted in partial uncoupling of mitochondria but no difference in mitochondrial membrane potential. The results demonstrate that the important environmental pollutant Cd2+ induces apoptosis in oyster immune cells and does so through a mitochondria/caspase-independent pathway,suggesting that a novel, perhaps ancient, apoptotic pathway is active in these cells. Furthermore, it appears that the observed decrease in ATP production during apoptosis is not due to the loss of the mitochondrial proton-motive force but is more likely to be due to inhibition of the F0/F1-ATPase and/or mitochondrial ADP/ATP or substrate transport.