Low Mitochondrial Free Radical Production Per Unit O₂Consumption Can Explain the Simultaneous Presence of High Longevity and High Aerobic Metabolic Rate in Birds

Abstract

Birds are unique since they can combine a high rate of oxygen consumption at rest with a high maximum life span (MLSP). The reasons for this capacity are unknown. A similar situation is present in primates including humans which show MLSPs higher than predicted from their rates of O2 consumption. In this work rates of oxygen radical production and O2 consumption by mitochondria were compared between adult male rats (MLSP = 4 years) and adult pigeons (MLSP = 35 years), animals of similar body size. Both the O2 consumption of the whole animal at rest and the O2 consumption of brain, lung and liver mitochondria were higher in the pigeon than in the rat. Nevertheless, mitochondrial free radical production was 2-4 times lower in pigeon than in rat tissues. This is possible because pigeon mitochondria show a rate of free radical production per unit O2 consumed one order of magnitude lower than rat mitochondria: bird mitochondria show a lower free radical leak at the respiratory chain. This result, described here for the first time, can possibly explain the capacity of birds to simultaneously increase maximum longevity and basal metabolic rate. It also suggests that the main factor relating oxidative stress to aging and longevity is not the rate of oxygen consumption but the rate of oxygen radical production. Previous inconsistencies of the rate of living theory of aging can be explained by a free radical theory of aging which focuses on the rate of oxygen radical production and on local damage to targets relevant for aging situated near the places where free radicals are continuously generated.

Protein and lipid oxidative damage and complex I content are lower in the brain of budgerigar and canaries than in mice. Relation to aging rate

“…The studies in birds are especially illustrative because these animals live much longer than mammals of similar body size and metabolic rate, contradictory to the old Brate-ofliving theory of aging^ (Pearl 1928). In spite of their high rates of oxygen consumption, birds have low rates of mitochondrial free radical production in brain (Barja et al 1994;Barja and Herrero 1998) and other major organs. Both small birds and large mammals have low rates of mitochondrial ROS production Barja et al 1994;Barja 1997, 1998), in agreement with their slow aging rates, whereas metabolic rate is slow in large mammals but high in small birds.…”

“…In spite of their high rates of oxygen consumption, birds have low rates of mitochondrial free radical production in brain (Barja et al 1994;Barja and Herrero 1998) and other major organs. Both small birds and large mammals have low rates of mitochondrial ROS production Barja et al 1994;Barja 1997, 1998), in agreement with their slow aging rates, whereas metabolic rate is slow in large mammals but high in small birds. Thus, maximum longevity correlates better with the mitochondrial rate of ROS generation than with overall metabolic rate.…”

Antioxidants in eggs of great tits Parus major from Chernobyl and hatching success

“…The combination of these facts suggests that birds have evolved a range of physiological mechanisms that allow them to successfully cope with high levels of oxidative stress. In fact, low production of free radicals per unit of oxygen consumption by mitochondria may explain these eVects (Barja et al 1994).…”

Response of Sod-2 enzyme activity to selection for high voluntary wheel running

“…Some evidence supports the idea that longterm exercise training may also increase the level of antioxidant enzyme activity, as well as generally improving Heredity the health of an individual while aging (Jenkins et al, 1984;Ji et al, 1986Ji et al, , 1990Ji et al, , 1991. Indeed, much evidence now supports oxidative damage as a probable proximate mechanism of senescence in mammals and insects (Sohal and Orr, 1992;Agarwal and Sohal, 1993;Barja et al, 1994;Orr and Sohal, 1994;Sohal et al, 1995;Sohal and Weindruch, 1996;Beckman and Ames, 1998).…”