Temperature adaptation in two bivalve species from different thermal habitats: energetics and remodelling of membrane lipids

Abstract

SUMMARY We compared lipid dynamics and the physiological responses of blue mussels Mytilus edulis, a cold-adapted species, and oysters Crassostrea virginica, a warmer-water species, during simulated overwintering and passage to spring conditions. To simulate overwintering, animals were held at 0°C, 4°C and 9°C for 3 months and then gradually brought to and maintained at 20°C for 5 weeks to simulate spring–summer conditions. Changes in lipid class and fatty acid composition were related to clearance rate and oxygen consumption. We found major differences between species in triglyceride (TAG) metabolism during overwintering. Mussels used digestive gland TAG stores for energy metabolism or reproductive processes during the winter, whereas oysters did not accumulate large TAG stores prior to overwintering. Mussel TAG contained high levels of 20:5n-3 compared to levels in oysters and in the diet. This may help to counteract the effect of low temperature by reducing the melting point of TAG and thus increasing the availability of storage fats at low temperature. Mussels seemed better able to mobilise 20:5n-3 and 18:4n-3 than other fatty acids. We also found that both bivalves underwent a major remodelling of membrane phospholipids. The unsaturation index decreased in the gills and digestive glands of both species during the early stages of warming, principally due to decreases in 22:6n-3 and 20:5n-3. In digestive glands, the unsaturation index did not increase with decreasing temperature beyond a threshold attained at 9°C whereas a perfect negative relationship was observed in gills, as predicted by homeoviscous adaptation. The presence of digestive enzymes and acids in the digestive gland microenvironment may lead to specific requirements for membrane stability. That oysters had lower metabolic rates than mussels coincides with a lower unsaturation index of their lipids, as predicted by Hulbert's theory of membranes as metabolic pacemakers. Both species showed increased 20:4n-6 levels in their tissues as temperature rose,suggesting an increasing availability of this fatty acid for eicosanoid biosynthesis during stress responses. The contrast between the species in TAG dynamics and the similarity of their phospholipid remodelling emphasises the essential functional role of membrane phospholipid structure and the contrasting use of TAG by oysters and mussels during overwintering.

Fatty acid and stable isotope biomarkers suggest microbe‐induced differences in benthic food webs between depths

“…Environmental characteristics that could potentially differ between the depths studied include temperature, light, and pressure. Temperature can affect FA of bivalves (Pernet et al 2007) and MSI signatures of euphausiids (Frazer et al 1997), likely as a function of growth and metabolism. However, our data suggest that temperatures do not differ greatly between these depths (D. O. Duggins unpubl.)…”

Remodeling of membrane lipids in gills of adult hard clam Mercenaria mercenaria during declining temperature

“…Fatty acid methyl esters (FAME) from total lipids (mainly phospholipids) were prepared using 2% H 2 SO 4 in methanol (Lepage & Roy 1984). Gas chromatograph parameters and the procedure for FAME identification and analysis have previously been described (Pernet et al 2007b). …”

The effect of seasonal temperature variation on behaviour and metabolism in the freshwater mussel (Unio tumidus)

“…Combined, these factors help maintain swimming performance in the face of thermal variation, and thus maintain the ability to catch prey or out-swim predators. Although these phenomena have not been as well explored in aquatic invertebrates, changes are known to occur in mitochondrial structure (Lurman et al, 2010a,b) and the membrane lipid composition (Pernet et al, 2007) as a result of acclimatization. While at the whole animal level, this can result in changes in (scallop) swimming mechanics (Bailey and Johnston, 2005) and recovery duration from swimming (Guderley, 2004a), or the acute thermal tolerance limits in freshwater mussels (Galbraith et al, 2012).…”

“…In general, oxygen consumption in a range of marine and freshwater bivalves exhibits no thermal compensation at low to intermediate temperatures and only minimal evidence of compensation at intermediate to high temperatures characteristic of their natural thermal range (Alexander and McMahon, 2004;Baker and Hornbach, 2001;Hornbach et al, 1983;Huebner, 1982;Newell et al, 1977;Newell and Pye, 1970;Pernet et al, 2007Pernet et al, , 2008Resgalla et al, 2007;Riascos et al, 2012;Tankersley and Dimock, 1993;Widdows, 1973).…”