Extracellular manganese as a redox mediator and matrix binder in cyanobacterial photoelectrochemistry

The model organism Synechocystis sp. PCC6803 is routinely employed in biophotoelectrochemical systems for the study of extracellular electron transport and the production of solar electricity, chemicals and fuels. The precise mechanism of electron export in Synechocystis is still under debate; NADPH has previously been proposed as the endogenous mediator, whilst others suggest the involvement of metal ions such as Mn and Fe species. Here, we first tested the hypothesis that NADPH acts as an electron mediator during biophotoelectrochemistry of Synechocystis cells on indium tin oxide (ITO) electrodes. We found that under standard conditions NADPH does not exhibit properties of an electron mediator between the cyanobacteria and electrode. Second, we investigated the role of extracellular Mn ions in cyanobacterial photocurrent production. The ability of endogenous and exogenous Mn ions to enhance photocurrents was tested, and up to 40-fold enhancements of were observed following the electrochemical production of localised oxidised Mn pools. We observed the contraction of the extracellular polymeric matrix upon oxidation of Mn ions, marked by increased cell-cell and cell-electrode interactions. These results provide future directions for increasing cyanobacteria-electrode adhesion and overall photocurrent output in these bioelectrochemical systems.