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

Significance

Employing renewable electric energy to power material–microbe hybrids for chemical synthesis has emerged as a promising approach for a sustainable society. When the materials and microbes are not in physical contact with each other, it is commonly assumed that the materials component that facilitates an electron transfer mediated by redox molecules like H ₂, does not serve to perturb microbial metabolism significantly. However, this study revealed that the electrochemical system can induce a fortuitous metabolic rewiring in planktonic S. ovata cells and an increased efficiency of utilizing provided reducing equivalents for CO ₂ fixation. This observation underscores the importance of revisiting existing assumptions of materials–biology interaction and adopting a more holistic approach to understand the underlying mechanisms at material-microbe interfaces.

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.