Multiple roles of released c‐type cytochromes in tuning electron transport and physiological status of Geobacter sulfurreducens

Abstract

AbstractDissimilatory metal‐reducing bacteria (DMRB) can transfer electrons to extracellular insoluble electron acceptors and play important roles in geochemical cycling, biocorrosion, environmental remediation, and bioenergy generation. c‐type cytochromes (c‐Cyts) are synthesized by DMRB and usually transported to the cell surface to form modularized electron transport conduits through protein assembly, while some of them are released as extracellularly free‐moving electron carriers in growth to promote electron transport. However, the type of these released c‐Cyts, the timing of their release, and the functions they perform have not been unrevealed yet. In this work, after characterizing the types of c‐Cyts released by Geobacter sulfurreducens under a variety of cultivation conditions, we found that these c‐Cyts accumulated up to micromolar concentrations in the surrounding medium and conserved their chemical activities. Further studies demonstrated that the presence of c‐Cyts accelerated the process of microbial extracellular electron transfer and mediated long‐distance electron transfer. In particular, the presence of c‐Cyts promoted the microbial respiration and affected the physiological state of the microbial community. In addition, c‐Cyts were observed to be adsorbed on the surface of insoluble electron acceptors and modify electron acceptors. These results reveal the overlooked multiple roles of the released c‐Cyts in acting as public goods, delivering electrons, modifying electron acceptors, and even regulating bacterial community structure in natural and artificial environments.