Nature and Value of Freely Dissolved EPS Ecosystem Services: Insight into Molecular Coupling Mechanisms for Regulating Metal Toxicity

Abstract

Extracellular polymeric substances (EPSs) dispersed in natural waters play a significant role in relieving impacts to microbial survival associated with heavy metal release, yet little is known about the association of freely dissolved EPS ecosystem services with metal transformation in natural waters. Here, we demonstrate that dispersive EPSs mitigate the metal toxicity to microbial cells through an associative coordination reaction. Microtitrimetry coupled with fluorescence spectroscopy ascribes the combination of freely dissolved EPSs from Escherichia coli (E. coli) with Cu/Cd to a coordination reaction associated with chemical static quenching. Fourier transform infrared spectroscopy (FTIR), X-ray photoelectron spectroscopy (XPS), and computational chemistry confirm that carboxyl residues in protein-like substances of the EPSs are responsible for the coordination. Frontier molecular orbitals (MOs) of a deprotonated carboxyl integrate with the occupied d orbitals of Cu and/or d, s orbitals of Cd to form metal-EPS complexes. Microcosmic systems show that because the metal-EPS complexes decrease cellular absorbability of metals, E. coli survivals increase by 4.3 times for Cu and 1.6 times for Cd, respectively. Based on bonding energies for six metals-EPS coordination, an associative toxic effect further confirms that increased bonding energies facilitate retardation of metals in the EPS matrix, protecting against E. coli apoptosis.

Effects of magnetic biochar-microbe composite on Cd remediation and microbial responses in paddy soil

“…The inoculation of bacteria into soil decreases Cd toxicity by binding of Cd with soil functional groups (i.e., sulfhydryl, carboxyl and amide groups) and chelation by bacterial extracellular polymers and soil organic acids, which are all directly affected by soil properties (Shou et al, 2018;Ma et al, 2011). Bacterial/biochar composites increased the immobilization of Cd more than biochar alone, by increasing bacterial absorption capability in soil due to the alteration of soil properties.…”

Revealing taxon-specific heavy metal-resistance mechanisms in denitrifying phosphorus removal sludge using genome-centric metaproteomics

“…Specifically, metal-resistance genes (MRGs) are those having experimentally evidenced merits to decrease the carrier's susceptibility to metals [11]. Besides, microbes are shown to relieve heavy metals' toxicity by producing extracellular polymeric substance (EPS) [12,13], outermembrane vesicles [14], inorganic polyphosphates (polyP) [15], and metallophores [16,17], or regulating outer membrane permeability [18]. On the one hand, MRGs are mainly retrieved from studies performed on model organisms such as Escherichia coli, Pseudomonas aeruginosa, and Saccharomyces cerevisiae [10,11].…”

Role of bacterial cell surface sulfhydryl sites in cadmium detoxification by Pseudomonas putida

“…Microorganisms, such as bacteria, can be sensitive to relatively low concentrations of toxic metals, 89 and they have developed multiple defense strategies to protect cells from toxic metals, such as cell 90 surface metal sequestration, metal efflux systems, intracellular metal sequestration, and metal 91 redox transformation (Gadd and Griffiths, 1978;Nies, 1999;Chandrangsu et al, 2017;Shou et al, 2018). Understanding the metal detoxification systems of bacteria is crucial in order to determine the environmental impacts of metal pollution on ecosystems and to develop appropriate strategies for a variety of applications, such as bioremediation (Shamim, 2018;Liu et al, 2019), water disinfection (Li et al, 2008), antimicrobial design (Turner, 2017), and biosynthesis of nanomaterials (Wadhwani et al, 2016).…”

“…In most cases, metals must enter bacterial cells to cause toxic effects (Nies, 1999). Therefore, blocking toxic metals before they cross cell membranes, e.g., immobilizing metals within the cell envelope or on extracellular polymeric substances (EPS) (Gadd and Griffiths, 1978;Shou et al, 2018) becomes an effective approach for lowering the bioavailability of toxic metals. Bacterial cell envelopes and cell-bound EPS molecules (which together we refer to here as cell surfaces) can adsorb a wide range of metals due to the presence of abundant functional groups (metal binding sites) on molecules within cell surfaces, such as carboxyl, phosphoryl and sulfhydryl sites (Beveridge and Murray, 1976;Liu and Fang, 2002;Fein et al, 2019).…”