Bio-driven Fe bond restructuring in bio-iron systems enhances electron transfer for chain elongation

Area of Science:

• Biotechnology
• Biochemistry
• Materials Science

Background:

• Medium-chain fatty acid (MCFA) biosynthesis is often limited by extracellular electron transfer.
• Iron-based systems show promise for enhancing this process, but their mechanisms are not fully understood.

Purpose of the Study:

• To investigate the structural characteristics and dynamic evolution of iron-based electron shuttles.
• To identify key factors influencing electron transfer and MCFA production in bio-iron systems.
• To elucidate the atomic-level microbial mechanisms governing iron-based electron shuttles.

Main Methods:

• Testing various iron species (Fe3O4, Fe2O3, FeCO3, iron powder) for extracellular electron transfer and MCFA production.
• Utilizing partial least squares regression and characterization analysis to identify key structural features.
• Employing X-ray absorption fine structure (XAFS) analysis and Marcus theory to study electron transfer dynamics.

Main Results:

• Fe3O4 demonstrated superior extracellular electron transfer and MCFA production.
• Microorganisms can transform iron powder and Fe2O3 into Fe3O4 via redox cycling.
• The Fe(III)-O-Fe(II) structure was identified as crucial for electron shuttle function.
• Bio-driven FeO bond shortening and FeFe bond elongation were linked to reduced reorganization energy and expanded electron transfer networks, respectively.

Conclusions:

• Fe3O4 is a highly effective electron shuttle for MCFA biosynthesis.
• Microbial redox cycling plays a significant role in optimizing iron-based electron shuttles.
• Understanding atomic-level iron structures and dynamics provides a foundation for designing bioinspired materials and improving bio-iron systems.