Ultrafast electron transfer kinetics at semiconductor-microbe interface: key to efficient extracellular photoelectron utilization

ABSTRACT The key limiting factors on energy conversion efficiency in semiconductor-microbe hybrid systems remain inadequately understood. This study investigates the impact of ultrafast electron transfer kinetics at Cd x Zn 1- x S/ Shewanella oneidensis MR-1 interfaces on the overall efficiency of hybrid systems. The reduction efficiency of direct blue 71 dye by Cd x Zn 1- x S/MR-1 is significantly enhanced under light, leveraging the synergy of extracellular photoelectron transfer in various Cd x Zn 1- x S nanoparticles and associated redox pathways in MR-1. Notably, CdS/MR-1 achieved a 98% reduction compared to 31% for ZnS/MR-1 after 1 hour, despite ZnS exhibiting a more favorable conduction band potential of −1.37 V vs normal hydrogen electrode (NHE). Time-resolved spectra and density functional theory calculations reveal that the efficiency advantages of CdS/MR-1 are attributed to its longer photoelectron lifetime (1.14 ± 0.12 ps vs 0.18 ± 0.03 ps for ZnS/MR-1) and higher electron mobility (119.71 cm²/V·s for CdS/MR-1 vs 62.47 cm²/V·s for ZnS/MR-1), providing MR-1 with superior kinetic advantages in utilizing photoelectron energy. Additionally, experiments with exogenous cytochrome c demonstrate its crucial role in modulating extracellular and intracellular electron transfer kinetics at the Cd x Zn 1- x S/MR-1 interface. Transcriptomic analysis reveals similar photoelectron transfer pathways in CdS/MR-1 and ZnS/MR-1, supporting that CdS/MR-1′s superior efficiency stems from kinetic advantages at the interface, leading to greater bioavailable photoelectron accumulation. These findings underscore the importance of optimizing photoelectron transfer kinetics to enhance extracellular photoelectron utilization efficiency in semiconductor-microbe hybrid systems. IMPORTANCE The synergy of light-sensitive semiconductor elements (e.g., natural minerals) and microbes in natural matrices enhances biological functions and opens a wide range of biotechnological possibilities. Given the extremely short lifetimes of photoelectrons and rapid transfer rates at semiconductor-microbe interface, understanding this ultrafast electron transfer process is essential for elucidating the mechanism of extracellular photoelectron utilization and optimizing system efficiency. Our study demonstrates that Shewanella oneidensis MR-1 can benefit from photoelectrons through ultrafast electron transfer pathways, similar to photosynthetic systems. For microbes to efficiently utilize these photoelectrons before charge recombination on an ultrafast timescale, a prolonged photoelectron lifetime is kinetically advantageous. Our findings indicate that the superior efficiency of the CdS/MR-1 hybrid system is driven by kinetic advantages rather than thermodynamic factors. This foundational study is crucial for optimizing the energetics of semiconductor-microbe hybrid systems and expands our understanding of microbial energy metabolism.