Inducible variation in anaerobic energy metabolism reflects hypoxia tolerance across the intertidal and subtidal distribution of the Pacific oyster ( Crassostrea gigas )

Abstract

Pacific oyster (Crassostrea gigas) distribute a steep gradient of environmental stress between intertidal and subtidal habits and provide insight into population-scale patterns and underlying processes of variation in physiological tolerance. In this study, 1-year-old-F oysters, collected from subtidal and intertidal habitats, were obtained after common garden experiment. Genetic differentiation and physiological responses under air exposure were examined to determine whether they had evolved into local adapted subpopulations. Mortality rate, anaerobic glycolysis metabolism, and energy status indicated that oyster had initiated metabolism depression and anaerobic glycolysis metabolism in both intertidal and subtidal oysters under air exposure. However, the subtidal oysters displayed the larger energy metabolism depressions and the earlier anaerobic glycolysis responses. This may indicate that subtidal oysters were more sensitives to hypoxia stress, which may lead the higher mortality rate under long term of air exposure. Based on a common garden experimental design, we propose that this diversification may have a genetic background. Overall, the clear differences between intertidal and subtidal oysters under air exposure have provided an important reference for their aquaculture and transportation used in commercial production.

Thermotolerance Divergence Revealed by the Physiological and Molecular Responses in Two Oyster Subspecies of Crassostrea gigas in China

“…This transition is supported by OCLTT models that highlight disorders in the oxygen supply, declines in aerobic scope and the onset of anaerobic metabolism at extreme temperatures (Pörtner, 2010; Sokolova et al, 2012). In line with our finding, this evidence was also reported in similar studies through key enzyme activities ( PK , PEPCK ), anaerobiosis end products and the expression patterns of metabolic genes (Li A. et al, 2017; Li L. et al, 2018; Meng et al, 2018). In the current study, the southern oysters exhibited a higher SMR at 32–40°C, which indicated a greater ability of this subspecies to provide sufficient aerobic energy that is required for somatic maintenance than its northern counterpart.…”

“…In addition, the calculated Q 10 values indicated no dependence of SMR on temperature above the ABTs. Moreover, the accumulation of anaerobiosis end products indicated the switch from aerobic to anaerobic mitochondrial metabolism and defined the critical thresholds (Michaelidis et al, 2005; Tagliarolo and McQuaid, 2015; Meng et al, 2018). Consequently, ABT may serve as a marker of the critical temperature at which metabolism changes for aerobic to anaerobic (Sokolova et al, 2012).…”

“…When animals are faced with moderate stress, metabolism and ATP turnover accelerate to provide the required maintenance cost and compensate for the increased energy demands for the protection of physiological functions (Paschke et al, 2018). During extreme stress, aerobic metabolism is impaired, and aerobic metabolism switches to anaerobic metabolism to compensate for declines in aerobic energy stores (Pörtner, 2012; Sokolova et al, 2012); however, this type of metabolism is less efficient than aerobic metabolism and is followed by end-product accumulation and intracellular acidosis (Bayne, 2017; Meng et al, 2018). Overall, physiological divergence across latitudinal gradients reflects the result of adaptive differences and can also be caused by neutral variation and various types of flexibility (Somero, 2010; Dowd et al, 2015).…”

Characterization, fluctuation and tissue differences in nutrient content in the Pacific oyster ( Crassostrea gigas ) in Qingdao, northern China

“…Pyruvate kinase, PFK and PGK in the glycolysis pathway had similar expression patterns as those for GP and GDE, which may reflect their whereabouts after glycogen decomposition. Comparable results were observed that subtidal oysters show higher GLUT and HK expression levels, as well as PK, PFK and PGK to generate more energy to cope with air exposure (Meng, Wang, Li, & Zhang, ). Sodium glucose co‐transporter expression in gonad tissue in this study showed higher expression levels in May, which supports that SGLT was significantly higher than under food deprivation, as demonstrated by natural breeding or artificially conditioned experiments (Hanquet et al, ).…”

Effects of intermittent hypoxia on the cell survival and inflammatory responses in the intertidal marine bivalves Mytilus edulis and Crassostrea gigas

“…Marine intertidal bivalves such as the Pacific oyster Crassostrea gigas and the blue mussel Mytilus edulis are common organisms in the intertidal, estuarine and shallow coastal habitats in the northern hemisphere where they can be exposed to frequent oxygen fluctuations ranging from near-anoxia to hyperoxia during diurnal and tidal cycles, as well as to seasonal hypoxia (Breitburg et al, 2015;de Zwaan and Putzer, 1985;Diaz and Rosenberg, 2008;Richards, 2011). Of these two species, the Pacific oysters are considered more tolerant to abiotic stressors, including prolonged hypoxia, than the blue mussels (David et al, 2005;Le Moullac et al, 2007;Meng et al, 2018;Zhang et al, 2012Zhang et al, , 2016. Our recent study showed that C. gigas survives longer in severe hypoxia and is better at maintaining the intracellular homeostasis of intermediate metabolites (including the free amino acids, urea cycle and purine metabolism intermediates) during H-R than M. edulis (Haider et al, 2020).…”