Age-related cellular changes in the long-lived bivalve A. islandica

Abstract

One of the biggest challenges to studying causes and effects of aging is identifying changes in cells that are related to senescence instead of simply the passing of chronological time. We investigated two populations of the longest living non-colonial metazoan, Arctica islandica, with lifespans that differed sixfolds. Of four investigated parameters (nucleic acid oxidation, protein oxidation, lipid oxidation, and protein instability), only nucleic acid oxidation increased with age and correlated with relative lifespan. Nucleic acid oxidation levels increased significantly faster and were significantly higher in the shorter-lived than the longer-lived population. In contrast, neither protein oxidation, lipid oxidation, nor protein stability changed over time. Protein resistance to unfolding stress when treated with urea was significantly lower overall in the shorter-lived population, and lipid peroxidation levels were higher in the longer-lived population. With the exception of nucleic acid oxidation, damage levels of A. islandica do not change with age, indicating excellent cellular maintenance in both populations. Since correlations between nucleic acid oxidation and age have also been shown previously in other organisms, and nucleic acid oxidation accumulation rate correlates with relative age in both investigated populations, nucleic acid oxidation may reflect intrinsic aging mechanisms.

Fig. 1

Nucleic acid damage in gill tissue of Baltic Sea (circles) and Icelandic (triangles) animals. a DNA and b RNA oxidation in both populations over age. Significance of the slopes, i.e., increase of oxidation with increasing age is displayed within the graphs. c DNA and d RNA oxidation calculated over the relative lifespan of both populations

Fig. 2

Lipid peroxidation in gill tissue of Baltic Sea and Icelandic A. islandica. Lipid peroxidation over age quantified as F₂-isoprostanes relative to total wet weight in a the Baltic Sea (circles) and b the Icelandic (triangles) population (scales are different for each population)

Fig. 3

Protein damage in gill tissue of Baltic Sea (circles) and Icelandic (triangles) A. islandica. Relative quantification of protein carbonyls (in FTC fluorescence) to total protein content (Coomassie absorbance) in a soluble and b insoluble proteins. c Protein resistance with age to 1 M urea unfolding stress measured as BisANS-coupled fluorescent units relative to total protein content in Icelandic samples. d Protein resistance to 1 M urea stress of Baltic Sea animals. e Mean levels of protein resistance to urea stress of all measured BS and IC individuals ± SEM. Equal letters indicate nonsignificant differences among populations and treatments, whereas different letters indicate significances at the p ≤ 0.05 level