Whereas the antimicrobial mechanisms of silver have been extensively studied and exploited for numerous applications, little is known about the associated bacterial adaptation and defense mechanisms that could hinder disinfection efficacy or mitigate unintended impacts to microbial ecosystem services associated with silver release to the environment. Here, we demonstrate that extracellular polymeric substances (EPS) produced by bacteria constitute a permeability barrier with reducing constituents that mitigate the antibacterial activity of silver ions (Ag(+)). Specifically, manipulation of EPS in Escherichia coli suspensions (e.g., removal of EPS attached to cells by sonication/centrifugation or addition of EPS at 200 mg L(-1)) demonstrated its critical role in hindering intracellular silver penetration and enhancing cell growth in the presence of Ag(+) (up to 0.19 mg L(-1)). High-resolution transmission electron microscopy (HRTEM) combined with X-ray photoelectron spectroscopy (XPS) and energy-dispersive spectrometry (EDS) analyses showed that Ag(+) was reduced to silver nanoparticles (AgNPs; 10-30 nm in diameter) that were immobilized within the EPS matrix. Fourier transform infrared (FTIR) and (13)C nuclear magnetic resonance (NMR) spectra suggest that Ag(+) reduction to AgNPs by the hemiacetal groups of sugars in EPS contributed to immobilization. Accordingly, the amount and composition of EPS produced have important implications on the bactericidal efficacy and potential environmental impacts of Ag(+).
BackgroundBecause of the increasing quantity and high toxicity to humans of polycyclic aromatic hydrocarbons (PAHs) in the environment, several bioremediation mechanisms and protocols have been investigated to restore PAH-contaminated sites. The transport of organic contaminants among plant cells via tissues and their partition in roots, stalks, and leaves resulting from transpiration and lipid content have been extensively investigated. However, information about PAH distributions in intracellular tissues is lacking, thus limiting the further development of a mechanism-based phytoremediation strategy to improve treatment efficiency.ResultsPyrene exhibited higher uptake and was more recalcitrant to metabolism in ryegrass roots than was phenanthrene. The kinetic processes of uptake from ryegrass culture medium revealed that these two PAHs were first adsorbed onto root cell walls, and they then penetrated cell membranes and were distributed in intracellular organelle fractions. At the beginning of uptake (< 50 h), adsorption to cell walls dominated the subcellular partitioning of the PAHs. After 96 h of uptake, the subcellular partition of PAHs approached a stable state in the plant water system, with the proportion of PAH distributed in subcellular fractions being controlled by the lipid contents of each component. Phenanthrene and pyrene primarily accumulated in plant root cell walls and organelles, with about 45% of PAHs in each of these two fractions, and the remainder was retained in the dissolved fraction of the cells. Because of its higher lipophilicity, pyrene displayed greater accumulation factors in subcellular walls and organelle fractions than did phenanthrene.ConclusionsTranspiration and the lipid content of root cell fractions are the main drivers of the subcellular partition of PAHs in roots. Initially, PAHs adsorb to plant cell walls, and they then gradually diffuse into subcellular fractions of tissues. The lipid content of intracellular components determines the accumulation of lipophilic compounds, and the diffusion rate is related to the concentration gradient established between cell walls and cell organelles. Our results offer insights into the transport mechanisms of PAHs in ryegrass roots and their diffusion in root cells.
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 (Au) 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 Auwas 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 Au reduction, reflecting the predominance of the extracellular matrix in Au reduction. XPS, UV-vis, and FTIR analyses corroborated that Au 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 Au 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.
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