Evolution of a biological thermocouple by adaptation of cytochrome c oxidase in a subterrestrial metazoan, Halicephalobus mephisto

Commun Biol. 2024 Sep 28;7(1):1214. doi: 10.1038/s42003-024-06886-z.

Abstract

In this study, we report a biological temperature-sensing electrical regulator in the cytochrome c oxidase of the Devil Worm, Halicephalobus mephisto. This extremophile metazoan was isolated 1.3 km underground in a South African goldmine, where it adapted to heat and potentially to hypoxia, making its mitochondrial sequence a likely target of adaptational change. We obtained the complete mitochondrial genome sequence of this organism and show through dN/dS analysis evidence of positive selection in H. mephisto cytochrome c oxidase subunits. Seventeen of these positively selected amino acid substitutions were located in proximity to the H- and K-pathway proton channels of the complex. Surprisingly, the H. mephisto cytochrome c oxidase completely shuts down at low temperatures (20 °C), leading to a 4.8-fold reduction in the transmembrane proton gradient (ΔΨm) compared to optimal temperature (37 °C). Direct measurement of oxygen consumption found a corresponding 4.6-fold drop at 20 °C compared to 37 °C. Correspondingly, the lifecycle of H. mephisto takes four times longer at low temperature than at higher. This elegant evolutionary adaptation creates a finely-tuned mitochondrial temperature sensor, allowing this ectothermic organism to maximize its reproductive success across varying environmental temperatures.

MeSH terms

  • Adaptation, Physiological / genetics
  • Animals
  • Biological Evolution
  • Electron Transport Complex IV* / genetics
  • Electron Transport Complex IV* / metabolism
  • Genome, Mitochondrial
  • Nematoda* / classification
  • Nematoda* / enzymology
  • Nematoda* / genetics
  • Nematoda* / physiology
  • Phylogeny
  • Temperature

Substances

  • Electron Transport Complex IV