ATP production from electricity with a new-to-nature electrobiological module

Electricity is paramount to the technical world and plays an increasingly important role as a future energy carrier. Yet, it is not widely used to directly power biological systems. Here, we designed a new-to-nature electrobiological module, the acid/aldehyde ATP cycle (AAA cycle), for the direct conversion of electrical energy into ATP. The AAA cycle contains a minimum set of enzymes and does not require membrane-based charge separation. Realizing a propionate-based version of the AAA cycle, we demonstrate continuous, electricity-driven regeneration of ATP and other energy storage molecules from −0.6 V vs. SHE at 2.7 μmol cm−2 h−1 and faradaic efficiencies of up to 47%. Notably, the AAA cycle is compatible with complex cell-free systems, such as in vitro transcription/translation, powering the processing of biological information directly from electricity. This new link between the technical and biological worlds opens several possibilities for future applications in synthetic biology, electrobiotechnology, and bioelectrocatalysis.