Cytochrome gene expression shifts in Geobacter sulfurreducens to maximize energy conservation in response to changes in redox conditions

Previous studies have identified that Geobacter sulfurreducens has three different electron transfer pathways for respiration, and it switches between these pathways to adapt to the redox potential of its electron acceptor. However, only a small fraction of the electron carriers from each pathway have been identified. In this study, we combined electrochemical and gene expression data to identify electron carriers in the inner membrane, periplasm, outer membrane, and exterior of the cell that may be induced by the use of the three different electron transfer pathways. Cyclic voltammetry was performed on thin biofilms grown on anodes poised at different redox potentials, providing a quantitative assessment of the relative use of three electron-transfer pathways in each condition (catalytic midpoint potentials (EKAs) of-0.227 V [Low],-0.15 V [Medium],-0.1 V [High] vs. SHE). Transcriptomic analyses as a function of electrochemical signals or fumarate utilization showed differential induction in inner membrane (Medium: cbcL), periplasmic (Low: ppcB/ppcE, Medium: ppcA), outer membrane (Low: extA/extC, Medium: extJ/extK, Fumarate: extF/extG), and extracellular (Medium: omcZ, High/Fumarate: omcS/omcT) cytochromes, suggesting the pathway signals are associated with complex transcriptomic responses in genes across the electron transfer pathway. Our method combining electrochemical modeling and transcriptomics could be adapted to better understand electron transport in other electroactive organisms with complex metabolisms.

Automated summary

This study combines electrochemical and gene expression data to identify electron carriers in Geobacter sulfurreducens that may be induced by the use of three different electron transfer pathways. Cyclic voltammetry experiments on biofilms grown at different redox potentials quantitatively assess the relative use of these pathways. Transcriptomic analyses reveal complex transcriptomic responses across the electron transfer pathways. This method can be adapted to study electron transport in other electroactive organisms with complex metabolisms.