The ocean quahog Arctica islandica is one of the longest-living and slowest-growing marine bivalves. The oldest specimens obtained for the present study approached 200 yr. To achieve such a long lifespan, accumulation of oxidative damage markers in tissues must ideally be maintained at low levels over time, because the accumulating debris disturbs cellular functions. We investigated shell growth and cellular aging in an Icelandic population of A. islandica. Specifically, we analyzed protein carbonyl concentration as a marker for the oxidative deterioration of tissue proteins, and the accumulation of the fluorescent age pigment lipofuscin over quahog lifetime in gill, mantle and adductor muscle. The very slow growth rates of A. islandica correlate with very efficient maintenance of body proteins compared to other, faster aging bivalves. Lipofuscin granules accumulated mainly in connective tissues of gill and mantle. Lowest lipofuscin accumulation was found in the adductor muscle, and there, only outside the myofibrils. Consistent with the pleiotropic theory of aging, A. islandica seems to trade slow growth and late onset of reproduction for a very efficient autophagic potential that mitigates oxidative damage accumulation and supports long lifetime and presumably reproduction in very old ocean quahog.
SUMMARYArctica islandica is the longest-lived non-colonial animal found so far, and reaches individual ages of 150years in the German Bight (GB) and more than 350years around Iceland (IC). Frequent burrowing and physiological adjustments to low tissue oxygenation in the burrowed state are proposed to lower mitochondrial reactive oxygen species (ROS) formation. We investigated burrowing patterns and shell water partial pressure of oxygen (P O2 ) in experiments with live A. islandica. Furthermore, succinate accumulation and antioxidant defences were recorded in tissues of bivalves in the normoxic or metabolically downregulated state, as well as ROS formation in isolated gills exposed to normoxia, hypoxia and hypoxia/reoxygenation. IC bivalves burrowed more frequently and deeper in winter than in summer under in situ conditions, and both IC and GB bivalves remained burrowed for between 1 and 6days in laboratory experiments. Shell water P O2 was <5kPa when bivalves were maintained in fully oxygenated seawater, and ventilation increased before animals entered the state of metabolic depression. Succinate did not accumulate upon spontaneous shell closure, although shell water P O2 was 0kPa for over 24h. A ROS burst was absent in isolated gills during hypoxia/reoxygenation, and antioxidant enzyme activities were not enhanced in metabolically depressed clams compared with normally respiring clams. Postponing the onset of anaerobiosis in the burrowed state and under hypoxic exposure presumably limits the need for elevated recovery respiration upon surfacing and oxidative stress during reoxygenation.
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