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Unexpected metabolic rewiring of CO <sub>2</sub> fixation in H <sub>2</sub> -mediated materials–biology hybrids

Yongchao Xie, Sevcan Erşan, Xun Guan, Jingyu Wang, Jihui Sha, Shuangning Xu, James A. Wohlschlegel, Junyoung O. Park, Chong Liu

2023Proceedings of the National Academy of Sciences29 citationsDOIOpen Access PDF

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.

Topics & Concepts

Synthetic biologyOxidizing agentAbiotic componentBiologyMicroorganismElectrochemistryBiochemical engineeringEnvironmental chemistryNanotechnologyBacteriaChemistryComputational biologyMaterials scienceEcologyOrganic chemistryGeneticsEngineeringPhysical chemistryElectrodeMicrobial Fuel Cells and BioremediationCO2 Reduction Techniques and CatalystsElectrochemical sensors and biosensors