Unexpected metabolic rewiring of CO 2 fixation in H 2 -mediated materials–biology hybrids

Abstract

A hybrid approach combining water-splitting electrochemistry and H 2 -oxidizing, CO 2 -fixing microorganisms offers a viable solution for producing value-added chemicals from sunlight, water, and air. The classic wisdom without thorough examination to date assumes that the electrochemistry in such a H 2 -mediated process is innocent of altering microbial behavior. Here, we report unexpected metabolic rewiring induced by water-splitting electrochemistry in H 2 -oxidizing acetogenic bacterium Sporomusa ovata that challenges such a classic view. We found that the planktonic S. ovata is more efficient in utilizing reducing equivalent for ATP generation in the materials–biology hybrids than cells grown with H 2 supply, supported by our metabolomic and proteomic studies. The efficiency of utilizing reducing equivalents and fixing CO 2 into acetate has increased from less than 80% of chemoautotrophy to more than 95% under electroautotrophic conditions. These observations unravel previously underappreciated materials’ impact on microbial metabolism in seemingly simply H 2 -mediated charge transfer between biotic and abiotic components. Such a deeper understanding of the materials–biology interface will foster advanced design of hybrid systems for sustainable chemical transformation.