Proton conductance and fatty acyl composition of liver mitochondria correlates with body mass in birds

Abstract

The proton conductance of isolated liver mitochondria correlates significantly with body mass in mammals, but not in ectotherms. To establish whether the correlation in mammals is general for endotherms or mammal-specific, we measured proton conductance in mitochondria from birds, the other main group of endotherms, using birds varying in mass over a wide range (nearly 3000-fold), from 13 g zebra finches to 35 kg emus. Respiratory control ratios were higher in mitochondria from larger birds. Mitochondrial proton conductance in liver mitochondria from birds correlated strongly with body mass [respiration rate per mg of protein driving proton leak at 170 mV being 44.7 times (body mass in g)(-0.19)], thus suggesting a general relationship between body mass and proton conductance in endotherms. Mitochondria from larger birds had the same or perhaps greater surface area per mg of protein than mitochondria from smaller birds. Hence, the lower proton conductance was caused not by surface area changes but by some change in the properties of the inner membrane. Liver mitochondria from larger birds had phospholipid fatty acyl chains that were less polyunsaturated and more monounsaturated when compared with those from smaller birds. Phospholipid fatty acyl polyunsaturation correlated positively and monounsaturation correlated negatively with proton conductance. These correlations echo those seen in mammalian liver mitochondria, suggesting that they too are general for endotherms.

Life and Death: Metabolic Rate, Membrane Composition, and Life Span of Animals

“…As it is in mammals, the proton leak of isolated liver mitochondria is allometrically related to body mass in birds (37). The PUFA content of avian liver mitochondrial membranes is negatively related to body mass, and this was predominantly due to decreased levels of n-6 PUFA as birds increased in body mass (37). This differs from the situation in mammals where it is n-3 PUFA variation that is primarily responsible for body size trends in liver mitochondrial membrane composition (289).…”

“…As for mammals, membrane-associated processes are significant components of respiration rate of avian hepatocytes and, while the total respiration rate decreases with body mass, the relative contribution of mitochondrial ATP production, mitochondrial proton leak, and nonmitochondrial processes is unchanged (91). As it is in mammals, the proton leak of isolated liver mitochondria is allometrically related to body mass in birds (37). The PUFA content of avian liver mitochondrial membranes is negatively related to body mass, and this was predominantly due to decreased levels of n-6 PUFA as birds increased in body mass (37).…”

“…176). However, recently it has been shown that one aspect of cell composition, namely, membrane fatty acid composition, does vary in a systematic manner with body size in mammals (69,164) and in birds (37,162). It has also been shown that membrane fatty acid composition is related to MLSP (266,271,272,(275)(276)(277).…”

Interspecific correlation between red blood cell mitochondrial ROS production, cardiolipin content and longevity in birds

“…It matches a previous finding in mammals that larger species have lower densities of mitochondria per gram of liver and are longer-lived (Passos et al 2007b). Moreover, it has already been suggested that differences in mitochondria proton conductance between bird species is more likely to be explained by differences in inner-membrane properties than by variations in the amount of membranes (Brand et al 2003). Altogether, our results suggest that longer lifespan in bird species may be associated both with lower densities of mitochondria per RBC and with greater amount of cardiolipin in their mitochondrial inner membrane, which are both expected to reduce mitochondrial ROS production.…”

Explaining longevity of different animals: is membrane fatty acid composition the missing link?

“…Small bird species have more polyunsaturated membrane lipids than do larger birds in skeletal muscle (Hulbert et al 2002), heart (Szabo et al 2006), and liver mitochondria (Brand et al 2003), as well as kidney (A.J. Hulbert, unpublished).…”