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Competitive advantage of oxygen-tolerant bioanodes of Geobacter sulfurreducens in bioelectrochemical systems.

ABSTRACT: Oxidative stress greatly limits current harvesting from anode biofilms in bioelectrochemical systems yet insufficient knowledge of the antioxidant responses of electricigens prevents optimization. Using Geobacter sulfurreducens PCA as a model electricigen, we demonstrated enhanced oxygen tolerance and reduced electron losses as the biofilms grew in height on the anode. To investigate the molecular basis of biofilm tolerance, we developed a genetic screening and isolated 11 oxygen-tolerant (oxt) strains from a library of transposon-insertion mutants. The aggregative properties of the oxt mutants promoted biofilm formation and oxygen tolerance. Yet, unlike the wild type, none of the mutants diverted respiratory electrons to oxygen. Most of the oxt mutations inactivated pathways for the detoxification of reactive oxygen species that could have triggered compensatory chronic responses to oxidative stress and inhibit aerobic respiration. One of the mutants (oxt10) also had a growth advantage with Fe(III) oxides and during the colonization of the anode electrode. The enhanced antioxidant response in this mutant reduced the system's start-up and promoted current harvesting from bioanodes even in the presence of oxygen. These results highlight a hitherto unknown role of oxidative stress responses in the stability and performance of current-harvesting biofilms of G. sulfurreducens and identify biological and engineering approaches to grow electroactive biofilms with the resilience needed for practical applications.

SUBMITTER: Speers AM

PROVIDER: S-EPMC8242959 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Multiheme cytochromes have been implicated in Geobacter sulfurreducens extracellular electron transfer (EET). These proteins are potential targets to improve EET and enhance bioremediation and electrical current production by G. sulfurreducens. However, the functional characterization of multiheme cytochromes is particularly complex due to the co-existence of several microstates in solution, connecting the fully reduced and fully oxidized states. Over the last decade, new strategies have been developed to characterize multiheme redox proteins functionally and structurally. These strategies were used to reveal the functional mechanism of G. sulfurreducens multiheme cytochromes and also to identify key residues in these proteins for EET. In previous studies, we set the foundations for enhancement of the EET abilities of G. sulfurreducens by characterizing a family of five triheme cytochromes (PpcA-E). These periplasmic cytochromes are implicated in electron transfer between the oxidative reactions of metabolism in the cytoplasm and the reduction of extracellular terminal electron acceptors at the cell's outer surface. The results obtained suggested that PpcA can couple e(-)/H(+) transfer, a property that might contribute to the proton electrochemical gradient across the cytoplasmic membrane for metabolic energy production. The structural and functional properties of PpcA were characterized in detail and used for rational design of a family of 23 single site PpcA mutants. In this review, we summarize the functional characterization of the native and mutant proteins. Mutants that retain the mechanistic features of PpcA and adopt preferential e(-)/H(+) transfer pathways at lower reduction potential values compared to the wild-type protein were selected for in vivo studies as the best candidates to increase the electron transfer rate of G. sulfurreducens. For the first time G. sulfurreducens strains have been manipulated by the introduction of mutant forms of essential proteins with the aim to develop and improve bioelectrochemical technologies.

Project description:Biomineralization of Cu has been shown to control contaminant dynamics and transport in soils. However, very little is known about the role that subsurface microorganisms may play in the biogeochemical cycling of Cu. In this study, we investigate the bioreduction of Cu(II) by the subsurface metal-reducing bacterium Geobacter sulfurreducens Rapid removal of Cu from solution was observed in cell suspensions of G. sulfurreducens when Cu(II) was supplied, while transmission electron microscopy (TEM) analyses showed the formation of electron-dense nanoparticles associated with the cell surface. Energy-dispersive X-ray spectroscopy (EDX) point analysis and EDX spectrum image maps revealed that the nanoparticles are rich in both Cu and S. This finding was confirmed by X-ray absorption near-edge structure (XANES) and extended X-ray absorption fine structure (EXAFS) analyses, which identified the nanoparticles as Cu2S. Biomineralization of CuxS nanoparticles in soils has been reported to enhance the colloidal transport of a number of contaminants, including Pb, Cd, and Hg. However, formation of these CuxS nanoparticles has only been observed under sulfate-reducing conditions and could not be repeated using isolates of implicated organisms. As G. sulfurreducens is unable to respire sulfate, and no reducible sulfur was supplied to the cells, these data suggest a novel mechanism for the biomineralization of Cu2S under anoxic conditions. The implications of these findings for the biogeochemical cycling of Cu and other metals as well as the green production of Cu catalysts are discussed.IMPORTANCE Dissimilatory metal-reducing bacteria are ubiquitous in soils and aquifers and are known to utilize a wide range of metals as terminal electron acceptors. These transformations play an important role in the biogeochemical cycling of metals in pristine and contaminated environments and can be harnessed for bioremediation and metal bioprocessing purposes. However, relatively little is known about their interactions with Cu. As a trace element that becomes toxic in excess, Cu can adversely affect soil biota and fertility. In addition, biomineralization of Cu nanoparticles has been reported to enhance the mobilization of other toxic metals. Here, we demonstrate that when supplied with acetate under anoxic conditions, the model metal-reducing bacterium Geobacter sulfurreducens can transform soluble Cu(II) to Cu2S nanoparticles. This study provides new insights into Cu biomineralization by microorganisms and suggests that contaminant mobilization enhanced by Cu biomineralization could be facilitated by Geobacter species and related organisms.

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Competitive advantage of oxygen-tolerant bioanodes of Geobacter sulfurreducens in bioelectrochemical systems.

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