Extracellular Saccharide-Mediated Reduction of Au3+ to Gold Nanoparticles: New Insights for Heavy Metals Biomineralization on Microbial Surfaces

Biomineralization is a critical process controlling the biogeochemical cycling, fate, and potential environmental impacts of heavy metals. Despite the indispensability of extracellular polymeric substances (EPS) to microbial life and their ubiquity in soil and aquatic environments, the role played by EPS in the transformation and biomineralization of heavy metals is not well understood. Here, we used gold ion (Au3+) as a model heavy metal ion to quantitatively assess the role of EPS in biomineralization and discern the responsible functional groups. Integrated spectroscopic analyses showed that Au(3+)was readily reduced to zerovalent gold nanoparticles (AuNPs, 2-15 nm in size) in aqueous suspension of Escherichia coli or dissolved EPS extracted from microbes. The majority of AuNPs (95.2%) was formed outside Escherichia coli cells, and the removal of EPS attached to cells pronouncedly suppressed Au3+ reduction, reflecting the predominance of the extracellular matrix in Au3+ reduction. XPS, UV-vis, and FTIR analyses corroborated that Au3+ reduction was mediated by the hemiacetal groups (aldehyde equivalents) of reducing saccharides of EPS. Consistently, the kinetics of AuNP formation obeyed pseudo-second -order reaction kinetics with respect to the concentrations of Au3+ and the hemiacetal groups in EPS, with minimal dependency on the source of microbial EPS. Our findings indicate a previously overlooked, universally significant contribution of EPS to the reduction, mineralization, and potential detoxification of metal species with high oxidation state.