The extreme longevity of Arctica islandica is associated with increased peroxidation resistance in mitochondrial membranes

Abstract

Summary The deleterious reactive carbonyls released upon oxidation of polyunsaturated fatty acids in biological membranes are believed to foster cellular aging. Comparative studies in mammals and birds have shown that the susceptibility to peroxidation of membrane lipids peroxidation index (PI) is negatively correlated with longevity. Long‐living marine molluscs are increasingly studied as longevity models, and the presence of different types of lipids in the membranes of these organisms raises questions on the existence of a PI–longevity relationship. We address this question by comparing the longest living metazoan species, the mud clam Arctica islandica (maximum reported longevity = 507 year) to four other sympatric bivalve molluscs greatly differing in longevity (28, 37, 92, and 106 year). We contrasted the acyl and alkenyl chain composition of phospholipids from the mitochondrial membranes of these species. The analysis was reproduced in parallel for a mix of other cell membranes to investigate whether a different PI–longevity relationship would be found. The mitochondrial membrane PI was found to have an exponential decrease with increasing longevity among species and is significantly lower for A. islandica. The PI of other cell membranes showed a linear decrease with increasing longevity among species and was also significantly lower for A. islandica. These results clearly demonstrate that the PI also decreases with increasing longevity in marine bivalves and that it decreases faster in the mitochondrial membrane than in other membranes in general. Furthermore, the particularly low PI values for A. islandica can partly explain this species’ extreme longevity.

Thermal sensitivity and phenotypic plasticity of cardiac mitochondrial metabolism in European perch, Perca fluviatilis

“…and E.S., unpublished observation), consequently depressing cardiac metabolic activity (as indicated by reduced cardiac power output) as previously observed in Biotest fish (Ekström et al, 2016a). The higher level of SFA and lower content of PUFA also significantly contributed in the reduction of the peroxidation index (PI) of the membranes, which is known to be associated with a higher resistance to oxidative stress, as shown in bivalves (see Munro and Blier, 2012). This result is also in line with modified proportions of CI/CIV observed in the chronically warm Biotest population, which could also prevent high-temperature-induced ROS production in the warmacclimated Biotest fish (Banh et al, 2016;Blier et al, 2014).…”

Perspectives on the membrane fatty acid unsaturation/pacemaker hypotheses of metabolism and aging

“…Within birds, the same is true in membranes from liver mitochondria and skeletal muscle (Hulbert, 2005). Similarly, in bivalves, peroxidation index and DHA content of mitochondrial membranes decreased with increasing longevity (Munro and Blier, 2012). There have also been multiple comparisons of the peroxidation index of long and short-lived species: pigeons, naked mole rats, and humans have a lower peroxidation index and DHA content in the mitochondrial membranes of their livers and hearts than do rats, which have a shorter lifespan (Hulbert, 2006;Mitchell et al, 2007;Pamplona et al, 1999aPamplona et al, , 1996.…”

“…In the one study that separated mitochondria from other membranes and then used those other membranes, rather than whole tissue, to connect peroxidation index to longevity, the peroxidation index of mitochondrial membranes and the peroxidation index of non-mitochondrial membranes were both correlated with longevity in bivalves, though the correlation between mitochondrial peroxidation index and longevity was stronger (Munro and Blier, 2012).…”

Low hydrogen peroxide production in mitochondria of the long‐lived Arctica islandica: underlying mechanisms for slow aging

“…This concept has not been supported by comparative studies investigating antioxidant defenses (Hulbert et al, 2007). However, there is evidence that the mitochondrial ROS production rate is lower in long-lived species (hereafter referred to the ROS-longevity relation; reviewed in Barja, 2004), and that these species possess macromolecules (such as lipids and proteins) with a better intrinsic resistance to oxidation (Hulbert et al, 2007;Munro & Blier, 2012).…”