Mitochondrial ageing of a polar and a temperate mud clam

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Abstract

We investigated mitochondrial ageing in a temperate (Mya arenaria) and an Antarctic (Laternula elliptica) mud clam, with similar lifestyle (benthic filter feeders) but different maximum life spans (MLSP), 13 and 36 years, respectively. The short-lived temperate M. arenaria showed a more pronounced decrease in mitochondrial function (respiration, respiratory control ratio, proton leak, membrane potential) with age than the long-lived Antarctic L. elliptica. H2O2 generation rates at habitat temperature were far higher in the short-lived M. arenaria compared to L. elliptica. Reactive oxygen species (ROS) production as proportion of the mitochondrial oxygen consumption rate (%H2O2/O2) increased significantly with age in M. arenaria, whereas in L. elliptica the proportion remained unchanged. Lower rates of mitochondrial H2O2 generation were presumably due to mild uncoupling as L. elliptica mitochondria showed higher proton leak compared to M. arenaria mitochondria. The results are discussed in to the light of the “Free Radical-Rate of Living theory”, (Pearl, R., 1928. The Rate of Living. Alfred Knopf, New York; Harman, D., 1956. Aging: a theory based on free radical and radiation biology. J. Gerontol. 11, 298–300) and the “Uncoupling to Survive” hypothesis (Brand, M.D., 2000. Uncoupling to survive? The role of mitochondrial inefficiency in ageing. Exp. Gerontol. 35, 811–820).

Introduction

With the exception of some simple forms like hydra, planarians and turbellarians (Child, 1915, Balazs and Burg, 1962, Haranghy and Balazs, 1964, Martinez, 1998), all multicellular organisms age. Two theories link the process of ageing and the maximum life span (MLSP) of a species to mitochondrial oxygen free radical (ROS) formation:

  • (i)

    The “Free Radical-Rate of Living theory”, (Pearl, 1928, Harman, 1956) predicts a negative correlation between SMR and MLSP due to increased mitochondrial production of oxygen free radicals at higher standard metabolic rate (SMR) (Ku et al., 1993).

  • (ii)

    The “uncoupling to survive” hypothesis (Brand, 2000) is based on the same assumption of a negative correlation between ROS production and MLSP, but further predicts that mitochondrial uncoupling mechanisms may modulate reactive oxygen species (ROS) production, altering the strict dependency of ROS formation on SMR.

When comparing marine and freshwater ectotherms of similar lifestyle, several groups discovered higher MLSPs in species from permanently cold compared to temperate environments (Brey, 1991, Brey et al., 1995, Ziuganov et al., 2000, Cailliet et al., 2001, La Mesa and Vacchi, 2001). In Antarctica, marine ectotherms experience year round permanent cold temperatures between −1.9 and +2.0 °C and most species have lower SMRs than related species from temperate environments, where temperatures fluctuate from 0 to 18 °C (Clarke, 1983, Heilmayer et al., 2004). According to the “Free Radical-Rate of Living theory”, these lower SMRs and the correspondingly low ROS generation by aerobic mitochondrial activity might result in a slow down of physiological ageing and may explain the higher MLSP of polar ectotherms compared to their temperate relatives. However, aside from higher mitochondrial densities in several polar (Johnston et al., 1998) and subpolar species (Sommer and Pörtner, 2002), mitochondrial adaptations in the cold involve higher cristae densities and altered membrane fatty acid composition, that may modulate free radical leakage from mitochondria and compromise the simple relationship between SMR and MLSP (Archer and Johnston, 1991, Johnston et al., 1994, St.-Pierre et al., 1998, Sommer and Pörtner, 2002).

For an analysis of whether MLSP is set by the level of SMR and by associated differences in mitochondrial functioning in marine ectotherms, we investigated age dependent changes of mitochondrial energy coupling and ROS formation in isolated mitochondria from mantle tissue of the Antarctic mud clam Laternula elliptica (Pholadomyoida) and the North Sea mud clam Mya arenaria (Myoida). Both clams are representatives of the same ecotype (benthic filter feeders and burrowing clams) and important key species in their respective habitat, but have adapted to different temperature regimes over long evolutionary time scales (Soot-Ryen, 1952, Petersen et al., 1992, Jonkers, 1999). With a maximum age of approximately 36 years, L. elliptica has a three-fold longer MLSP than M. arenaria with ∼13 years MLSP. Although the animals belong to different bivalve subclasses their similarity in size, morphology and lifestyle should justify a comparison of physiological ageing parameters between both species.

Section snippets

Laternula elliptica

Antarctic L. elliptica were collected by divers in the Potter Cove, King George Island, South Shetland Island (62°14′S, 58°40′W) in November–February 2002/2003 at 5–10 m depths, 34 PSU and temperatures between −1 and +2 °C. Animals were maintained in aquaria with seawater from the cove at 0 °C for several days until they were used for experimentation. Water was exchanged once a week to ensure a good water quality and food supply. All measurements were carried out at the Dallmann-Laboratory, King

Age dependent changes in the function of isolated mitochondria

Oxygen consumption of mitochondria isolated from mantle tissue of the temperate M. arenaria and the polar mud clam L. elliptica at in situ temperatures are presented in Fig. 1.

A significant decline of respiratory capacity with chronological age was recorded in both species. The slope of the decrement was, however, more than two times steeper in M. arenaria than in L. elliptica mitochondria. This resulted in lower respiration rates of mitochondria isolated from aged M. arenaria compared to aged

Discussion

The present study clearly demonstrates age related changes of mitochondrial functions in both investigated bivalves. This is in line with other studies which found important changes in isolated mitochondria from aging humans (Trounce et al., 1989, Cooper et al., 1992, Boffoli et al., 1994), other vertebrates like rats (Nohl and Hegner, 1978, Ventura et al., 2002) and invertebrates (Sohal et al., 1995), see Shigenaga et al. (1994) for review. Moreover, Hagen et al. (1997) documented that

Conclusions

The results from this and a previous study (Philipp et al., 2005) explain a three-fold higher MLSP found in a polar compared to a temperate mud clam along the lines of two different ageing theories: the “Free Radical-Rate of Living theory “(Pearl, 1928, Harman, 1956) and the “Uncoupling to Survive” hypothesis (Brand, 2000). In line with the first theory, the longer-lived polar L. elliptica shows lower SMRs than the shorter-lived temperate M. arenaria (Philipp et al., 2005). On the other hand,

Acknowledgements

Rob Dekker and the Crew from the RV Navicula from the NIOZ kindly took E. Philipp on several sampling trips to collect M. arenaria. Many thanks to the Argentinean Divers, the Station Management of Jubany as well as Thomas Brey for scientific discussions, Timo Hirse and Oscar Gonzales for logistic as well as scientific support at the Argentinean Antarctic Base Jubany and in Bremerhaven. The study was supported by a student grant of the University of Bremen. We would like to thank three anonymous

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