Abstract

BackgroundUncoupling proteins (UCP) are evolutionary conserved mitochondrial carriers that control energy metabolism and therefore play important roles in several physiological processes such as thermogenesis, regulation of reactive oxygen species (ROS), growth control, lipid metabolism and regulation of insulin secretion. Despite their importance in various physiological processes, their molecular function remains controversial. The evolution and phylogenetic distribution may assist to identify their general biological function and structure-function relationships. The exact number of uncoupling protein genes in the fish genome and their evolution is unresolved.ResultsHere we report the first characterisation of UCP gene family members in sea bass, Dicentrarchus labrax, and then retrace the evolution of the protein family in vertebrates. Four UCP genes that are shared by five other fish species were identified in sea bass genome. Phylogenetic reconstitution among vertebrate species and synteny analysis revealed that UCP1, UCP2 and UCP3 evolved from duplication events that occurred in the common ancestor of vertebrates, whereas the novel fourth UCP originated specifically in the teleost lineage. Functional divergence analysis among teleost species revealed specific amino acid positions that have been subjected to altered functional constraints after duplications.ConclusionsThis work provides the first unambiguous evidence for the presence of a fourth UCP gene in teleost fish genome and brings new insights into the evolutionary history of the gene family. Our results suggest functional divergence among paralogues which might result from long-term and differential selective pressures, and therefore, provide the indication that UCP genes may have diverse physiological functions in teleost fishes. Further experimental analysis of the critical amino acids identified here may provide valuable information on the physiological functions of UCP genes.

Highlights

  • Uncoupling proteins (UCP) are evolutionary conserved mitochondrial carriers that control energy metabolism and play important roles in several physiological processes such as thermogenesis, regulation of reactive oxygen species (ROS), growth control, lipid metabolism and regulation of insulin secretion

  • Annotation and nomenclature of sea bass UCPs The blast search of stickleback UCP1 against sea bass genome shotgun and BACend sequences allows the identification of three scaffolds putatively containing a UCP gene, which are respectively assigned to sea bass chromosomes LG7, LG14 and LG13

  • UCP2 and UCP3 were predicted on chromosome LG14 and were found adjacent as previously demonstrated in many vertebrates including fish

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Summary

Introduction

Uncoupling proteins (UCP) are evolutionary conserved mitochondrial carriers that control energy metabolism and play important roles in several physiological processes such as thermogenesis, regulation of reactive oxygen species (ROS), growth control, lipid metabolism and regulation of insulin secretion. Despite their importance in various physiological processes, their molecular function remains controversial. The exact number of uncoupling protein genes in the fish genome and their evolution is unresolved. Uncoupling proteins (UCP) are evolutionary conserved proteins involved in the coupling mechanism of the electron transport chain to ATP synthesis which is driven by a proton gradient over the mitochondrial inner membrane. Heat production by mammalian UCP1 is crucial for non-shivering thermogenesis and cold-survival of rodents, hibernators and human infants [13] while the physiological role of the UCP1 orthologue in ectotherms is unclear

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