Spatially Resolved Charge Transfer Kinetics at the Quantum Dot-Microbe Interface Using Fluorescence Lifetime Imaging Microscopy

Microbe-semiconductor biohybrids formed by integrating complex microbial enzymatic machinery with programmable optoelectronic properties of semiconducting quantum dots (QDs) have introduced compelling prospects for future photosynthetic solar-to-chemical transformations. Bringing these prospects to fruition requires a firm foundational understanding of charge transfer mechanisms at the nano- bio interface. One challenge is that the transfer of photoexcited carriers from a QD to drive redox reactions in a proximate microbe involves a complex interplay of photochemical and physiochemical sub-processes, and the governing thermodynamic and kinetic factors are just beginning to emerge. The inherent heterogeneities of both the microbe and QD ensemble presents additional challenges challenge to establishing robust mechanistic understanding and to ultimately translate basic insights to design principles for advanced biohybrids. In this study, we leveraged advanced spectroscopic imaging tools (fluorescence lifetime imaging microscopy, FLIM) to interrogate charge transfer kinetics at the interface of a CdSe quantum dot (QD) film and <i>Shewanella oneidensis</i> microbes with sub-cellular spatial resolution. We focused on electron transport under fumarate-rich conditions and observed that both the intensity and lifetime of the QD’s photoluminescence decrease at on-cell and inter-cell positions relative to the off-cell background. These trends provide a map of electron transfer rates (in the range of 10⁸ to 10⁹ s^-1 ) from QDs to the <i>S. oneidensis</i> cells for terminal reduction of fumarate. Our analysis of spatially resolved charge transfer rates reveals the role of cooperative effects in small groups of microbes, i.e., working together, small communities <i>S. oneidensis</i> exhibit faster charge transfer than isolated microbes. We attribute the cooperative effects to nanowire extrusions from <i>S. oneidensis</i> that facilitate charge uptake. Light driven electron transfer rates define the photo-chemical efficiency limits of photosynthetic semiconductor biohybrids, and this study provides important progress towards characterizing these electron transfer rates with enhanced spatial resolution.