Cold counteracting membrane fatty acid remodeling is not expressed during quiescence in the bivalve Mercenaria mercenaria

Abstract

To counteract the effects of cold on the pace of membrane bound metabolic processes, winter active ectotherms decrease saturated fatty acids (SFAs) and/or increase highly unsaturated fatty acids (HUFAs) esterified to phospholipids. Whereas it has been shown that winter dormant species do not undergo this cold counteracting lipid remodeling, no studies have investigated winter facultative quiescent species. The northern quahog (Mercenaria mercenaria) enters quiescence conditional to temperature decreasing below 6–7°C. Previous studies have shown that the species can operate a cold counteracting lipid remodeling with temperatures decreasing from 22 to 8°C, but there is no evidence that further adjustments are made at lower temperatures during quiescence. This study was designed to precisely investigate if cold counteracting lipid remodeling is further operated by M. mercenaria after entrance into quiescence. Individuals were cultured together with two evolutionarily- related (veneroid) cold-tolerant species (Spisula solidissima and Arctica islandica), and exposed to a natural annual temperature change between 12°C and 2°C. Individuals of M. mercenaria were sampled in December (beginning of the 2°C winter temperature plateau), and all three species were sampled in April (end of 2°C plateau), and again in August (end of 12°C summer plateau). Gill membrane carbon chain composition (fatty acids + alkenyl chains) was analyzed separately (GC-MS + GC-FID) for mitochondria and other sources of membranes (non-mitochondrial). Valve opening was monitored visually in all species, and markers of lipoxidation (lipid hydroperoxides and TBARS) were measured during winter in M. mercenaria to investigate possible signs of stress. Below 6–7°C, individuals of M. mercenaria maintained valves closed, and markers of lipoxidation increased. Changes in membrane lipids were observed for this species; however, these were opposite to what would counteract the effects of cold. The chain fluidity index and mol% HUFA were higher in August (12°C) instead of April (2°C). In contrast, both cold tolerant species maintained filter-feeding activity during winter and operated a cold counteracting lipid remodeling of mitochondrial membranes. In April, chain fluidity index was higher for S. solidissima and mol% HUFA was higher for A. islandica as compared to August. Our results show that M. mercenaria do not further attempt at counteracting the effects of cold on membranes after entrance into quiescence. Adjusting the pace of membrane processes to that of the whole organisms through conditional cold counteracting lipid remodeling may benefit facultative active ectotherms.