Microbial Extracellular Polymeric Substances Reduce Ag<sup>+</sup> to Silver Nanoparticles and Antagonize Bactericidal Activity

Kang, Fuxing; Alvarez, Pedro J. J.; Zhu, Dongqiang

doi:10.1021/es403796x

Cited by 263 publications

(150 citation statements)

References 37 publications

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“…strain EPS-5028 (50). The presence of arabinose and mannose in the cell-bound EPS as revealed by the glycolysis analysis (see Table S1 in the supplemental material) may explain this high reducing power, given that these monosaccharides have been linked to the reductive capabilities of EPS purified from other bacteria (51). Interestingly, the fast reduction rate of Pu by EPS contrasts with the much slower kinetics and efficacy of Pu reduction by humic acids (52).…”

Section: Discussionmentioning

confidence: 99%

Interactions of Plutonium with Pseudomonas sp. Strain EPS-1W and Its Extracellular Polymeric Substances

Boggs

Jiao

Dai

et al. 2016

Appl Environ Microbiol

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Safe and effective nuclear waste disposal, as well as accidental radionuclide releases, necessitates our understanding of the fate of radionuclides in the environment, including their interaction with microorganisms. We examined the sorption of Pu(IV) and Pu(V) to Pseudomonas sp. strain EPS-1W, an aerobic bacterium isolated from plutonium (Pu)-contaminated groundwater collected in the United States at the Nevada National Security Site (NNSS) in Nevada. We compared Pu sorption to cells with and without bound extracellular polymeric substances (EPS). Wild-type cells with intact EPS sorbed Pu(V) more effectively than cells with EPS removed. In contrast, cells with and without EPS showed the same sorption affinity for Pu(IV). In vitro experiments with extracted EPS revealed rapid reduction of Pu(V) to Pu(IV). Transmission electron microscopy indicated that 2-to 3-nm nanocrystalline Pu(IV)O 2 formed on cells equilibrated with high concentrations of Pu(IV) but not Pu(V). Thus, EPS, while facilitating Pu(V) reduction, inhibit the formation of nanocrystalline Pu(IV) precipitates. IMPORTANCEOur results indicate that EPS are an effective reductant for Pu(V) and sorbent for Pu(IV) and may impact Pu redox cycling and mobility in the environment. Additionally, the resulting Pu morphology associated with EPS will depend on the concentration and initial Pu oxidation state. While our results are not directly applicable to the Pu transport situation at the NNSS, the results suggest that, in general, stationary microorganisms and biofilms will tend to limit the migration of Pu and provide an important Pu retardation mechanism in the environment. In a broader sense, our results, along with a growing body of literature, highlight the important role of microorganisms as producers of redox-active organic ligands and therefore as modulators of radionuclide redox transformations and complexation in the subsurface.T he civil production of nuclear energy and military production of nuclear materials have resulted in an estimated worldwide inventory of over 2,000 metric tons of plutonium (Pu) (1). This inventory continues to increase at a rate of approximately 70 metric tons per year as a result of global nuclear energy production (2). Due to its long half-life (24,100 years for 239 Pu) and high radiotoxicity (3), Pu is an important driver in public health risk assessments for nuclear waste repositories and radiologically contaminated sites. However, predicting how Pu behaves in the environment and ultimately calculating its human health risk are limited by our understanding of the dominant biogeochemical processes controlling its behavior.The behavior of Pu in the environment is strongly dependent on its oxidation state and concentration. Among all the actinides, Pu has one of the most complex chemical, redox, and surface sorption behaviors. At low concentrations, Pu can exist as aqueous species in the III, IV, V, and/or VI oxidation states, all of which have different solubilities (4), mineral sorption affinities (5-7), and hence...

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Section: Discussionmentioning

confidence: 99%

Interactions of Plutonium with Pseudomonas sp. Strain EPS-1W and Its Extracellular Polymeric Substances

Boggs

Jiao

Dai

et al. 2016

Appl Environ Microbiol

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“…Beyond the adverse effects this could have for the organisms, it impacts the speciation or distribution of silver in the environment in complex ways, and notably as silver species can enter the trophic chains and be spread among a wide variety of organisms [87]. In particular, most micro-organisms (bacteria, micro-algae and fungi) produce extracellular polymeric substances (EPS) [138]. Ag NPs and Ag + species can be immobilized by these EPS.…”

Section: Fate Of Silver Nanoparticles In the Environmentmentioning

confidence: 99%

Antibacterial activity of silver nanoparticles: A surface science insight

2015

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Summary Silver nanoparticles constitute a very promising approach for the development of new antimicrobial systems. Nanoparticulate objects can bring significant improvements in the antibacterial activity of this element, through specific effect such as an adsorption at bacterial surfaces. However, the mechanism of action is essentially driven by the oxidative dissolution of the nanoparticles, as indicated by recent direct observations. The role of Ag + release in the action mechanism was also indirectly observed in numerous studies, and explains the sensitivity of the antimicrobial activity to the presence of some chemical species, notably halides and sulfides which form insoluble salts with Ag + . As such, surface properties of Ag nanoparticles have a crucial impact on their potency, as they influence both physical (aggregation, affinity for bacterial membrane, etc.) and chemical (dissolution, passivation, etc.) phenomena. Here, we review the main parameters that will affect the surface state of Ag NPs and their influence on antimicrobial efficacy. We also provide an analysis of several works on Ag NPs activity, observed through the scope of an oxidative Ag + release.

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“…lular redox-active metabolites with suitable redox potentials, a view supported by the large number of bacterial species known to reduce Ag ϩ and other metal ions to nanoparticles (7)(8)(9)(10)(11)(12). Indeed, the reduction of Ag ϩ by extracellular polymeric substances of Escherichia coli with reduced bactericidal activity has recently been demonstrated (29).…”

Section: Fig 6 Pyocyanin Confers Resistance To Agmentioning

confidence: 99%

Pyocyanin Production by Pseudomonas aeruginosa Confers Resistance to Ionic Silver

Müller

Merrett

2014

Antimicrob Agents Chemother

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Silver in its ionic form (Ag ؉ ), but not the bulk metal (Ag 0 ), is toxic to microbial life forms and has been used for many years in the treatment of wound infections. The prevalence of bacterial resistance to silver is considered low due to the nonspecific nature of its toxicity. However, the recent increased use of silver as an antimicrobial agent for medical, consumer, and industrial products has raised concern that widespread silver resistance may emerge. Pseudomonas aeruginosa is a common pathogen that produces pyocyanin, a redox toxin and a reductant for molecular oxygen and ferric (Fe 3؉ ) ions. The objective of this study was to determine whether pyocyanin reduces Ag ؉ to Ag 0 , which may contribute to silver resistance due to lower bioavailability of the cation. Using surface plasmon resonance spectroscopy and scanning electron microscopy, pyocyanin was confirmed to be a reductant for Ag ؉ , forming Ag 0 nanoparticles and reducing the bioavailability of free Ag ؉ by >95% within minutes. Similarly, a pyocyanin-producing strain of P. aeruginosa (PA14) reduced Ag ؉ but not a pyocyanin-deficient (⌬phzM) strain of the bacterium. Challenge of each strain with Ag ؉ (as AgNO 3 ) gave MICs of 20 and 5 g/ml for the PA14 and ⌬phzM strains, respectively. Removal of pyocyanin from the medium strain PA14 was grown in or its addition to the medium that ⌬phzM mutant was grown in gave MICs of 5 and 20 g/ml, respectively. Clinical isolates demonstrated similar pyocyanin-dependent resistance to Ag ؉ . We conclude that pseudomonal silver resistance exists independently of previously recognized intracellular mechanisms and may be more prevalent than previously considered.

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Microbial Extracellular Polymeric Substances Reduce Ag⁺ to Silver Nanoparticles and Antagonize Bactericidal Activity

Cited by 263 publications

References 37 publications

Interactions of Plutonium with Pseudomonas sp. Strain EPS-1W and Its Extracellular Polymeric Substances

Interactions of Plutonium with Pseudomonas sp. Strain EPS-1W and Its Extracellular Polymeric Substances

Antibacterial activity of silver nanoparticles: A surface science insight

Pyocyanin Production by Pseudomonas aeruginosa Confers Resistance to Ionic Silver

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Microbial Extracellular Polymeric Substances Reduce Ag+ to Silver Nanoparticles and Antagonize Bactericidal Activity

Cited by 263 publications

References 37 publications

Interactions of Plutonium with Pseudomonas sp. Strain EPS-1W and Its Extracellular Polymeric Substances

Interactions of Plutonium with Pseudomonas sp. Strain EPS-1W and Its Extracellular Polymeric Substances

Antibacterial activity of silver nanoparticles: A surface science insight

Pyocyanin Production by Pseudomonas aeruginosa Confers Resistance to Ionic Silver

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Product

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Microbial Extracellular Polymeric Substances Reduce Ag⁺ to Silver Nanoparticles and Antagonize Bactericidal Activity