Energetic levels of psychrophiles comprising all domains of life are unusual in that they display increased intracellular ATP and ATP/ADP levels with declining temperature. Transcriptomic profiling of the glacial ice worm Mesenchytraeus solifugus has revealed unique 13- and 18-amino acid C-terminal extensions on the ATP6 subunit, which forms a major component of the ATP synthase proton pore. These extensions are positioned near the exit half-channel in the mitochondrial matrix and contain multiple alternating histidine residues, hypothesized to increase proton flux through ATP synthase. This hypothesis was tested by fusing ice worm ATP6 extensions to gammaproteobacterium Escherichia coli AtpB (orthologue of ATP6), after which a ∼5-fold increase in ATP synthesis was observed. This enhancement functioned only unidirectionally, with no change in ATP hydrolysis rates; neither did it confer any change to ATP synthase’s enzymatic response to temperature. Despite increases in ATP synthase efficacy, the extension did not provide additional growth or protein expression advantages. The extension conferred a similar increased enzymatic rate for ATP synthase in Caulobacter crescentus, an alphaproteobacterium with different genomic and protein organization. These findings suggest that the histidine-rich ATP6 C-terminal extensions found in glacier ice worms increase the ATP production rate and thus offer an avenue for identifying critical factors associated with ice worm adaptation.