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

Autor: Megan N. Guerin, TreVaughn S. Ellis, Mark J. Ware, Alexandra Manning, Ariana A. Coley, Ali Amini, Adaeze G. Igboanugo, Amaya P. Rothrock, George Chung, Kristin C. Gunsalus, John R. Bracht
Jazyk: angličtina
Rok vydání: 2024
Předmět:
Zdroj: Communications Biology, Vol 7, Iss 1, Pp 1-13 (2024)
Druh dokumentu: article
ISSN: 2399-3642
02816377
DOI: 10.1038/s42003-024-06886-z
Popis: 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 (ΔΨ m ) 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.
Databáze: Directory of Open Access Journals
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