PHOTOREDUCTION OF FUMARATE BY ZNS IS INITIATED BY ULTRAFAST ONE-ELECTRON TRANSFER

Photochemical reactions at mineral surfaces have been proposed as important steps in the origins of life. In particular, the photoexcitation of semiconductor minerals such as sphalerite (ZnS) by ultraviolet light generates electrons capable of driving reduction reactions in the reverse tricarboxylic acid (rTCA) cycle [1]. The rTCA cycle has been proposed as a precursor to the oxidative cycle found in modern mitochondria.

We used liquid chromatography coupled to mass spectrometry (LCMS) to investigate possible side reactions in the ZnS photocatalyzed steps of the rTCA cycle, finding a diversity of end products in most cases. However, the proton-coupled, two-electron reduction of fumarate to succinate occurred in high yield with no alternative products. We chose to study the mechanism of this plausible prebiotic reaction to determine the chemical and structural factors that enable a relatively complex multi-electron reaction to proceed with high selectivity.

We used ultrafast spectroscopic techniques to study the reaction in a regime in which 310-nm illumination generated a single excited electron per ZnS nanoparticle. Using transient mid-infrared spectroscopy we captured the formation and relaxation of excited electrons in ZnS and found that, in the presence of fumarate, electrons are lost to the organic molecule at sub-picosecond timescales. Consistent with these data, a new optical absorption feature appeared on the same timescale that could represent an intermediate organic product of the fumarate reduction.

Additionally, we observed a reduction of the fluorescence lifetime of photoexcited ZnS in the presence of fumarate, indicating that further interfacial electron transfer continues up to the ~100-picosecond timescale. Transient optical spectroscopy also showed the filling of mid-bandgap trap states in the ZnS, from which we were unable to detect further electron transfer to adsorbed fumarate. We derived a mechanistic scheme for the first steps of the reduction of fumarate on ZnS that incorporates all observations within ~7 ns, and propose two hypotheses for reaction completion. This work will constrain the potential early Earth environments that could facilitate photochemical transformation of metabolic organic molecules.

[1] X.V. Zhang et al. (2006) J. Photochem. and Photobiol. 185, 301-311.