Importance of c-Type cytochromes for U(VI) reduction by Geobacter sulfurreducens

Shelobolina, Evgenya S.; Coppi, Maddalena V.; Korenevsky, Anton; DiDonato, Laurie N.; Sullivan, Sara A.; Konishi, Hiromi; Xu, Huifang; Leang, Ching; Butler, Jessica; Kim, Byoung Chan; Lovley, Derek R.

doi:10.1186/1471-2180-7-16

Cited by 191 publications

(171 citation statements)

References 52 publications

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“…The chemical composition of the medium can influence the nature of the reduced U mineral (34). We used a bicarbonate buffer and conditions used in previous studies with G. sulfurreducens (13), whereas studies reporting uraninite formation used PIPES-buffered solutions (36) or bicarbonatebuffered uncontaminated groundwater (10). Evidence for the microbial reduction of U(VI) to nonuraninite U(IV) products is also emerging from field-scale studies (35,37), whereas uraninite formation has been linked to conditions of reduced bioreducing activities (38,39); this suggests that abiotic factors may contribute to the formation of uraninite.…”

Section: Discussion Physiological Relevance Of the Extracellular Redumentioning

confidence: 99%

“…However, mutations were often pleitrophic (14-16) and showed either no defect or only partial defects in the cell's ability to remove U(VI) (12,13). Interpretation was also difficult due to inconsistencies in the reported mutant phenotypes, with some mutations reportedly abolishing U(VI) removal activities, yet mutant cells showing extensive mineralization (13). Furthermore, these studies consistently showed that the U precipitated inside the cell envelope.…”

mentioning

confidence: 90%

“…Resting-cell suspensions were prepared as described elsewhere (13), except that cells were harvested from mid-logphase cultures (OD 600 , 0.3-0.5) and resuspended in 100 mL reaction buffer with 20 mM sodium acetate to a final OD 600 of 0.1. Heat-killed controls were prepared by autoclaving the cultures for 30 min.…”

Section: Methodsmentioning

confidence: 99%

“…The development of genetic tools in Geobacter sulfurreducens (11) motivated molecular studies to elucidate the biological mechanism behind this reaction. Because c-cytochromes are abundant in the cell envelope of Geobacter bacteria, studies focused on identifying extracytoplasmic c-cytochromes that could function as dedicated U reductases (12,13). However, mutations were often pleitrophic (14-16) and showed either no defect or only partial defects in the cell's ability to remove U(VI) (12,13).…”

mentioning

confidence: 99%

“…Because c-cytochromes are abundant in the cell envelope of Geobacter bacteria, studies focused on identifying extracytoplasmic c-cytochromes that could function as dedicated U reductases (12,13). However, mutations were often pleitrophic (14-16) and showed either no defect or only partial defects in the cell's ability to remove U(VI) (12,13). Interpretation was also difficult due to inconsistencies in the reported mutant phenotypes, with some mutations reportedly abolishing U(VI) removal activities, yet mutant cells showing extensive mineralization (13).…”

mentioning

confidence: 99%

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Extracellular reduction of uranium via Geobacter conductive pili as a protective cellular mechanism

Cologgi

Lampa-Pastirk

Speers

et al. 2011

Proc. Natl. Acad. Sci. U.S.A.

221

239

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The in situ stimulation of Fe(III) oxide reduction by Geobacter bacteria leads to the concomitant precipitation of hexavalent uranium [U(VI)] from groundwater. Despite its promise for the bioremediation of uranium contaminants, the biological mechanism behind this reaction remains elusive. Because Fe(III) oxide reduction requires the expression of Geobacter 's conductive pili, we evaluated their contribution to uranium reduction in Geobacter sulfurreducens grown under pili-inducing or noninducing conditions. A pilin-deficient mutant and a genetically complemented strain with reduced outer membrane c -cytochrome content were used as controls. Pili expression significantly enhanced the rate and extent of uranium immobilization per cell and prevented periplasmic mineralization. As a result, pili expression also preserved the vital respiratory activities of the cell envelope and the cell's viability. Uranium preferentially precipitated along the pili and, to a lesser extent, on outer membrane redox-active foci. In contrast, the pilus-defective strains had different degrees of periplasmic mineralization matching well with their outer membrane c -cytochrome content. X-ray absorption spectroscopy analyses demonstrated the extracellular reduction of U(VI) by the pili to mononuclear tetravalent uranium U(IV) complexed by carbon-containing ligands, consistent with a biological reduction. In contrast, the U(IV) in the pilin-deficient mutant cells also required an additional phosphorous ligand, in agreement with the predominantly periplasmic mineralization of uranium observed in this strain. These findings demonstrate a previously unrecognized role for Geobacter conductive pili in the extracellular reduction of uranium, and highlight its essential function as a catalytic and protective cellular mechanism that is of interest for the bioremediation of uranium-contaminated groundwater.

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Section: Discussion Physiological Relevance Of the Extracellular Redumentioning

confidence: 99%

mentioning

confidence: 90%

Section: Methodsmentioning

confidence: 99%

mentioning

confidence: 99%

mentioning

confidence: 99%

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Extracellular reduction of uranium via Geobacter conductive pili as a protective cellular mechanism

Cologgi

Lampa-Pastirk

Speers

et al. 2011

Proc. Natl. Acad. Sci. U.S.A.

221

239

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NMR studies of the interaction between inner membrane‐associated and periplasmic cytochromes from Geobacter sulfurreducens

et al. 2017

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Geobacter sulfurreducens is a dissimilatory metal-reducing bacterium with notable properties and significance in biotechnological applications. Biochemical studies suggest that the inner membrane-associated diheme cytochrome MacA and the periplasmic triheme cytochrome PpcA from G. sulfurreducens can exchange electrons. In this work, NMR chemical shift perturbation measurements were used to map the interface region and to measure the binding affinity between PpcA and MacA. The results show that MacA binds to PpcA in a cleft defined by hemes I and IV, favoring the contact between PpcA heme IV and the MacA high-potential heme. The dissociation constant values indicate the formation of a low-affinity complex between the proteins, which is consistent with the transient interaction observed in electron transfer complexes.

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Microbial Transformations of Radionuclides in the Subsurface

Marshall

Beliaev

Fredrickson

2009

Environmental Microbiology

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Importance of c-Type cytochromes for U(VI) reduction by Geobacter sulfurreducens

Abstract: Background: In order to study the mechanism of U(VI) reduction, the effect of deleting c-type cytochrome genes on the capacity of Geobacter sulfurreducens to reduce U(VI) with acetate serving as the electron donor was investigated.

Cited by 191 publications

References 52 publications

Extracellular reduction of uranium via Geobacter conductive pili as a protective cellular mechanism

Extracellular reduction of uranium via Geobacter conductive pili as a protective cellular mechanism

NMR studies of the interaction between inner membrane‐associated and periplasmic cytochromes from Geobacter sulfurreducens

Microbial Transformations of Radionuclides in the Subsurface

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