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1 Department of Animal Physiology, Biology Faculty, Philipps-University Marburg, Marburg, Hessen, Germany
2 Department of Inland Fisheries, Leibniz-Institute of Freshwater Ecology and Inland Fisheries, Berlin, Germany
* To whom correspondence should be addressed. E-mail: klingens{at}staff.uni-marburg.de.
Uncoupling proteins increase proton leakage across the inner mitochondrial membrane. Thereby uncoupling protein 1 (UCP1) in brown adipose tissue dissipates proton motive force as heat. This mechanism of nonshivering thermogenesis is considered as a monophyletic trait of endothermic placental mammals which emerged about 140 million years ago and provided a crucial advantage for life in the cold. The paralogues UCP2 and UCP3 are probably not thermogenic proteins but convey mild uncoupling which may serve to reduce the rate of mitochondrial ROS production. Both are present in endotherms (mammals and birds), but so far only UCP2 was identified in ectothermic vertebrates (fish and amphibia). The evolution of uncoupling proteins is of general interest in the search for the origin of mammalian UCP1-mediated nonshivering thermogenesis. We here show the presence of UCP1 and UCP3 in ectothermic teleost fish species using comparative genomics, phylogenetic inference, and gene expression analysis. In the Common Carp (Cyprinus carpio), UCP1 is predominantly expressed in the liver and strongly diminished in response to cold exposure, thus contrasting the cold-induced expression of mammalian UCP1 in brown adipose tissue. UCP3 mRNA is only found in carp skeletal muscle with expression levels increased five-fold in response to fasting. Our findings disprove the monophyletic nature of UCP1 in placental mammals and demonstrate that all three members of the core UCP family were already present before the divergence of ray-finned and lobe-finned vertebrate lineages about 420 million years ago.
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