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First published online June 29, 2006
Journal of Experimental Biology 209, i-a (2006)
Copyright © 2006 The Company of Biologists Limited
doi: 10.1242/jeb.02390
Inside JEB |
KEEPING SHARKS WARM IN THE COLD
kathryn{at}biologists.com
Packed into our tissues, microscopic mitochondria are the body's power-houses, consuming oxygen to generate the ATP that powers our every move. However, warm-blooded creatures (endotherms) also benefit from one of the organelle's by-products, heat, generated when the organelles leak protons. In fact, up to 25% of the basal metabolic rate of most warm-blooded creatures can be attributed to energy consumed topping up the mitochondrial leak. In contrast, metabolically active tissues in cold-blooded creatures (ectotherms) contain far fewer mitochondria, and they are proportionately smaller than those in gas-guzzling endotherms. As a result, it has been suggested that mitochondrial proton leak could be a key factor in the evolution of a warm-blooded lifestyle. But what about species that seem to straddle both warm and cold camps; have their mitochondria become specialised so that they too benefit from warming proton leak? Kathryn Dickson, Jeff Graham and their colleagues in southern California explain that some shark species are endothermic, while the rest are ectotherms. Could the mitochondria of these endothermic fish contribute to their warmth? To find out, Dickson and her colleagues measured proton leak rates from the tissues of warm shortfin makos and two ectothermic species (p. 2678).
But before the team could go fishing, Dickson set off for a summer in England, to join Martin Brand's Cambridge lab and master the technically challenging assays used to measure mitochondrial proton leak. Having returned to California, Dickson explains that proton leak rates can only be measured on freshly caught animals, so the team could only work on days when Chugey Sepulveda returned from fishing trips in the Pacific Ocean with a catch of endothermic shortfin makos and ectothermic blue sharks and leopard sharks. Knowing that makos maintain their liver and red muscle temperatures well above ambient temperatures, and that both tissues are metabolically active, the team isolated mitochondria from both tissues before measuring the organelle's respiration rates and membrane potential, and calculating the proton leak rates.
Surprisingly, the mitochondrial proton leak rates at the same membrane potential were essentially identical in all three sharks; that is that all three species pumped the same number of protons per milligram of protein at the same electric driving force. Dickson says `this suggests that mitochondria from endothermic tissues of the mako shark are not specialised for thermogenesis'.
However, the team noticed that the mako shark's red muscle oxygen consumption rates were much higher than their ectothermic cousins, suggesting that even though the mitochondria are not adapted for heat production, the increased respiration rate could increase mitochondrial proton leak sufficiently to contribute to the fish's endothermy. And when the team measured the mitochondrial density in all three fishes' livers and calculated the proton leak per gram of tissue, they realised that the endothermic shark's was almost twice that of the ectothermic sharks.
Having found that both red muscle and liver could contribute to mako's endothermy, despite their lack of specialised mitochondria, Dickson and Graham are curious to know whether the mitochondria of other endothermic fish contribute to the challenge of keeping them warm.
References
Duong, C. A., Sepulveda, C. A., Graham, J. B. and Dickson, K.
A. (2006). Mitochondrial proton leak rates in the slow,
oxidative myotomal muscle and liver of the endothermic shortfin mako shark
(Isurus oxyrinchus) and the ectothermic blue shark (Prionace
glauca) and leopard shark (Triakis semifasciata). J.
Exp. Biol. 209,2678
-2685.
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