The mitochondrial uncoupling proteins in early-branching animals: comparative analysis and transcriptional response to temperature in the jellyfish Stomolophus sp.2.

Uncoupling proteins (UCPs) are mitochondrial membrane proteins involved in metabolite transportation and proton translocation to the mitochondrial matrix. Seven UCP homologs have been reported in bilaterians; however, UCPs of early-branching animals (i.e., members of Cnidaria, Ctenophora, Placozoa, and Porifera) remain understudied. The presence of UCPs in the cnidarian jellyfish Stomolophus sp.2. was investigated, and its UCP homologs were compared with data from 49 other early-branching species to provide insights into their evolution. Three UCPs were identified in Stomolophus sp.2: UCP4, UCP5, and a novel cnidarian-specific homolog (cnUCP). In addition to cnidarians, placozoans and sponges share UCP4 and UCP5 homologs, while ctenophores lack these but possess three distinct UCPs, two of them related to UCP5. Results suggest that since UCP4 and UCP5 originated at least at the Animalia-Choanoflagellata node and considering the evolutionary gains of UCPs in Cnidaria and Ctenophora, the relevance of these proteins in mitochondrial functions deserves attention. Moreover, to infer the role of UCPs in Stomolophus sp.2 mitochondria, their structural characteristics were identified, and the temperature effect on their gene expression was evaluated. Whereas UCP4 and UCP5 genes showed higher expression at 23 °C, cnUCP was highly expressed at 33 °C, suggesting a potential role in the jellyfish thermal stress response. Besides their role in mitochondrial uncoupling and energy balance, the bilaterian UCPs may mitigate reactive oxygen species production during thermal stress. However, their role in early-branching lineages remains unclear. This study provides key data for future functional research on UCPs in early-branching animals under climate change.