Spontaneous assembly of microbial extracellular polymeric substances into microcapsules involved in trapping and immobilizing degradation-resistant oxoanions

Abstract

Despite the ubiquity of microbial extracellular polymeric substances (EPS) in soils and aquatic environments, the roles played by EPS in the nonreductive transformation of toxic and degradation-resistant oxoanions are poorly understood. Here, we used perchlorate, which is ubiquitous in surface environments, as an initiator to study the spontaneous assembly of EPS into microcapsules involved in trapping and immobilizing oxoanions. The results confirmed that ClO₄^- oxoanions could be rapidly trapped in 20 min by EPS extracted from a common Bacillus subtilis, whereas no chemical reduction of ClO₄^- occurred in 48 h. Integrated spectroscopic analyses with florescence quenching microtitration and theoretical models showed that amino functionalities of EPS are responsible for sequestering ClO₄^-, with lower pH values being more favorable to formation of EPS-ClO₄^- micelles. Combined molecular dynamics scheme with wave function analyses showed that besides amino residues, the protonated side-chain amino groups in the basic proteins have a greater capacity for sequestering ClO₄^- through a noncovalent H-bonding mechanism in which dissociable protons serve as the nodes to bridge ClO₄^-. A quantitative association between the number of hydrogen bonds and bioavailability revealed that immobilization by EPS mitigates the uptake of toxic oxoanions by forage ryegrass, reducing their risk exposure to edible produce. MAIN FINDING OF THE WORK: Micelles formed by freely dissolved EPS mitigate the uptake of toxic oxoanions by forage ryegrass.

Keywords: Extracellular polymeric substance; Microcapsule; Migration; Noncovalent H-bonding; Perchlorate.