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Reversing an Extracellular Electron Transfer Pathway for Electrode-Driven Acetoin Reduction.

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This study engineered a microbial electrosynthesis system in Shewanella oneidensis MR-1, using light and native proteins to convert electrical energy and CO2 into valuable organic compounds like 2,3-butanediol.

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Area of Science:

  • Microbial electrosynthesis
  • Synthetic biology
  • Bioelectrochemistry

Background:

  • Microbial electrosynthesis (MES) offers potential for renewable energy storage, carbon fixation, and valuable chemical production.
  • A key limitation in MES is the incomplete understanding of electron uptake mechanisms into microbial cells.
  • Shewanella oneidensis MR-1 possesses native pathways for extracellular electron transfer (EET) that can be harnessed for MES.

Purpose of the Study:

  • To engineer a functional MES platform in Shewanella oneidensis MR-1 by connecting an extracellular electrode to intracellular reduction reactions.
  • To elucidate and utilize the native Mtr pathway for electron transfer from an electrode to the quinone pool.
  • To overcome thermodynamic limitations for intracellular electron transfer to NAD+ using light-driven proton pumps and establish an electron sink for product formation.

Main Methods:

  • Leveraged the native Mtr protein complex in Shewanella oneidensis MR-1 for extracellular electron uptake from an electrode.
  • Utilized native NADH dehydrogenases to transfer electrons from the quinone pool to NAD+.
  • Incorporated proteorhodopsin as a light-driven proton pump to generate proton-motive force, driving unfavorable intracellular electron transfer.
  • Introduced a heterologous butanediol dehydrogenase (Bdh) for the reduction of acetoin to 2,3-butanediol, serving as an electron sink.

Main Results:

  • Demonstrated successful electron transfer from the electrode to intracellular NAD+ via the engineered pathway.
  • Confirmed electron flux is dependent on both light availability and acetoin concentration.
  • Observed maximum 2,3-butanediol production when both light and a poised electrode were present.
  • Identified hydrogen production as a competing electron sink in wild-type strains, with reduced competition in hydrogenase-deficient mutants.

Conclusions:

  • The engineered MES system effectively utilizes cathodic electrons for intracellular reduction, driven by light and native electron transfer pathways.
  • This work provides a foundation for genetically engineered MES platforms for targeted synthesis of valuable compounds using electrical energy.
  • Understanding and manipulating electron transfer routes is crucial for optimizing MES efficiency and expanding its applications.