A histidine-rich extension of the mitochondrial F0 subunit ATP6 from the ice worm Mesenchytraeus solifugus increases ATP synthase activity in bacteria.

Bioenergetic profiles of psychrophiles across domains of life are unusual in that intracellular ATP levels increase with declining temperature. Whole-transcriptome sequencing of the glacier ice worm Mesenchytraeus solifugus revealed a unique C-terminal extension on the ATP6 protein, which forms part of the proton pore of mitochondrial ATP synthase (Complex V). This extension, positioned near the proton exit pore, comprises alternating histidine residues thought to increase proton flux through Complex V leading to elevated ATP synthesis. To test this hypothesis, we fused the M. solifugus C-terminal extension to Escherichia coli AtpB (the ATP6 orthologue) and observed a ~ 5-fold increase in ATP synthesis. This enhancement was unidirectional as we observed no change to ATP hydrolysis rates. These findings offer an avenue for identifying critical factors associated with ice worm adaptation.