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

Dissimilatory 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.