Electron Transfer Pathways Stretching from the Extracellular to Intracellular Membrane in Biohybrids Enable Enhanced CO2 Upcycling to Malate

Abstract Microbial electrosynthesis (MES) empowers one-step conversion of CO2 to long-chain chemicals under mild conditions, enabling sustainable biomanufacturing and achievement of a circular carbon economy. Although the construction of biohybrids has been explored to enhance the inherently low efficiency of MES, whether the binding modes between nanomaterials and microorganisms dictating CO2 conversion efficiency remain elusive. To address this query, we constructed biohybrids with three distinct integration modes (namely, internalization, outer membrane-contact, and transenvelope) between nanomaterials and Shewanella, enabling to proceed CO2-to-malate conversion. Upon MES-driven CO2-to-malate conversion, the transenvelope biohybrid constituted by polydopamine and Shewanella achieved a marked gram-scale malate titer of 19.14 mmol/L, as a result of the distinctive transenvelope capacity of polydopamine stretching from the extracellular to the intracellular membrane. This transenvelope capacity imparts extended electron transfer pathways spanning from the cytoplasmic membrane to the extracellular space, significantly reducing interfacial barriers at the electrode-microorganism interface and greatly promoting NADH and ATP synthesis for malate synthesis, which can enhance NADH synthesis. This work proposes the construction of a transenvelope biohybrid to optimize microbial metabolism, offering an alternative for the efficient valorization of CO2 to carbon-negative long-chain chemicals.