Abstract

The mitochondrial oxidative stress theory of aging posits that membrane susceptibility to peroxidation and the organization of the electron transport system (ETS) linked with reactive oxygen species (ROS) generation are two main drivers of lifespan. While a clear correlation has been established from species comparative studies, the significance of these characteristics as potential modulators of lifespan divergences among populations of individual species is still to be tested. The bivalve Arctica islandica, the longest-lived non-colonial animal with a record lifespan of 507 years, possesses a lower mitochondrial peroxidation index (PI) and reduced H2O2 efflux linked to complexes I and III activities than related species. Taking advantage of the wide variation in maximum reported longevities (MRL) among 6 European populations (36–507 years), we examined whether these two mitochondrial properties could explain differences in longevity. We report no relationship between membrane PI and MRL in populations of A. islandica, as well as a lack of intraspecific relationship between ETS complex activities and MRL. Individuals from brackish sites characterized by wide temperature and salinity windows had, however, markedly lower ETS enzyme activities relative to citrate synthase activity. Our results highlight environment-dependent remodeling of mitochondrial phenotypes.

Highlights

  • Understanding the physiological determinants of lifespan in animals has been the focus of biologists and gerontologists over the past decades

  • Population grouping significantly explained the variability of lipid peroxidation susceptibility markers (PI, plasmalogens, DHA, n-3 and n-6 polyunsaturated FA (PUFA)) in the gills, but not in the mantle tissue

  • Our results show similarities between these two brackish sites, with only the peroxidation index (PI) in gill membranes being markedly lower in White Sea (WS) than Kiel Bay (KB) animals, whereas for all the other longevity-linked lipids, the distribution of the two populations were overlapping in the principal analysis (PCA)

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Summary

Introduction

Understanding the physiological determinants of lifespan in animals has been the focus of biologists and gerontologists over the past decades. Comparative studies suggest a role for mitochondrial structure and function associated with the aging process, in particular the management of reactive oxygen species (ROS) This evidence has been integrated into one unifying hypothesis, the “mitochondrial oxidative stress theory of aging” (MOSTA, reviewed in Blier et al, 2017). It points out, among others, the importance of cell membrane composition and the susceptibility of mitochondrial membrane lipids to oxidation peroxidation index (PI) as potentially causative parameters of cellular aging. The products of FA oxidation (reactive aldehydes) induce autocatalytic progression of lipid peroxidation that can further damage membrane proteins, PUFA chains and DNA This leads to impaired protein functions and DNA mutations and underlines the crucial role of membrane lipid composition for cellular integrity, with implications for organismal lifespan (Hulbert, 2010)

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