Mitochondrial form and function in the heart of the world’s longest living vertebrate: Fish environmental physiology: A tribute to John Fleng Steffensen

The life span of the Greenland shark (Somniosus microcephalus) is at least 272 years and may be as long as 500 years making this animal the longest living vertebrate on the planet. This extreme longevity is particularly interesting for cardiac studies, because aging is synonymous with heart disease in humans. Mitochondria are dynamic subcellular organelles whose individual shape, organisation, and function (including reactive oxygen species production) is known to change with age. Thus, the focus of this study was to combine electron microscopy imaging and machine learning approaches in cardiac tissue from Greenland shark, aged between ~30 and ~210 years, to determine how mitochondrial form and function change with age. Both two- and three-dimensional electron microscopy image analysis correlated in showing that mitochondrial volume densities were similar among individuals regardless of age. In contrast, image analysis showed a marked increase in inner mitochondrial membrane (IMM) content in larger (and thus presumably older) sharks. Metallomics showed that copper-levels were low in Greenland sharks compared with mammals and the catshark and did not change with age, which may indicate that the copper-based Complex IV of the mitochondrial respiratory-chain is less abundant in this species. Together these data could indicate that mitochondria of older Greenland sharks increase IMM as a mean to facilitate oxygen diffusion rather than to facilitate aerobic capacity. Functional studies are required to support this contention and to shed greater light on the role of mitochondria in this model of extreme aging.