Lack of physiological evidence for cytochrome filaments functioning as conduits for extracellular electron transfer

• Published in: mBio 2024-05, Vol.15 (5), p.e0069024-e0069024
• Main Authors: Schwarz, Ingrid A, Alsaqri, Baha, Lekbach, Yassir, Henry, Kathryn, Gorman, Sydney, Woodard, Trevor, Dion, Laura, Real, Lauren, Holmes, Dawn E, Smith, Jessica A, Lovley, Derek R
• Format: Article
• Language: English
• Subjects: Cytochromes - genetics; Cytochromes - metabolism; electromicrobiology; Electron Transport; extracellular electron transfer; Ferric Compounds - metabolism; Fimbriae Proteins - genetics; Fimbriae Proteins - metabolism; Fimbriae, Bacterial - genetics; Fimbriae, Bacterial - metabolism; Geobacter; Geobacter - genetics; Geobacter - metabolism; geomicrobiology; microbial nanowires; Oxidation-Reduction; Physiology and Metabolism; Research Article
• ISSN: 2150-7511; 2150-7511
• DOI: 10.1128/mbio.00690-24

Extracellular cytochrome filaments are proposed to serve as conduits for long-range extracellular electron transfer. The primary functional physiological evidence has been the reported inhibition of Fe(III) oxide reduction when the gene for the filament-forming cytochrome OmcS is deleted. Here we report that the OmcS-deficient strain from that original report reduces Fe(III) oxide as well as the wild-type, as does a triple mutant in which the genes for the other known filament-forming cytochromes were also deleted. The triple cytochrome mutant displayed filaments with the same 3 nm diameter morphology and conductance as those produced by heterologously expressing the PilA pilin gene. Fe(III) oxide reduction was inhibited when the pilin gene in cytochrome-deficient mutants was modified to yield poorly conductive 3 nm diameter filaments. The results are consistent with the concept that 3 nm diameter electrically conductive pili (e-pili) are required for long-range extracellular electron transfer. In contrast, rigorous physiological functional evidence is lacking for cytochrome filaments serving as conduits for long-range electron transport. Unraveling microbial extracellular electron transfer mechanisms has profound implications for environmental processes and advancing biological applications. This study on challenges prevailing beliefs on cytochrome filaments as crucial components thought to facilitate long-range electron transport. The discovery of an OmcS-deficient strain's unexpected effectiveness in Fe(III) oxide reduction prompted a reevaluation of the key conduits for extracellular electron transfer. By exploring the impact of genetic modifications on ' performance, this research sheds light on the importance of 3-nm diameter electrically conductive pili in Fe(III) oxide reduction. Reassessing these mechanisms is essential for uncovering the true drivers of extracellular electron transfer in microbial systems, offering insights that could revolutionize applications across diverse fields.