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c-Type Cytochrome-Dependent Formation of U(IV) Nanoparticles by Shewanella oneidensis

Modern approaches for bioremediation of radionuclide contaminated environments are based on the ability of microorganisms to effectively catalyze changes in the oxidation states of metals that in turn influence their solubility. Although microbial metal reduction has been identified as an effective...

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Autores principales: Marshall, Matthew J, Beliaev, Alexander S, Dohnalkova, Alice C, Kennedy, David W, Shi, Liang, Wang, Zheming, Boyanov, Maxim I, Lai, Barry, Kemner, Kenneth M, McLean, Jeffrey S, Reed, Samantha B, Culley, David E, Bailey, Vanessa L, Simonson, Cody J, Saffarini, Daad A, Romine, Margaret F, Zachara, John M, Fredrickson, James K
Formato: Texto
Lenguaje:English
Publicado: Public Library of Science 2006
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC1526764/
https://www.ncbi.nlm.nih.gov/pubmed/16875436
http://dx.doi.org/10.1371/journal.pbio.0040268
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author Marshall, Matthew J
Beliaev, Alexander S
Dohnalkova, Alice C
Kennedy, David W
Shi, Liang
Wang, Zheming
Boyanov, Maxim I
Lai, Barry
Kemner, Kenneth M
McLean, Jeffrey S
Reed, Samantha B
Culley, David E
Bailey, Vanessa L
Simonson, Cody J
Saffarini, Daad A
Romine, Margaret F
Zachara, John M
Fredrickson, James K
author_facet Marshall, Matthew J
Beliaev, Alexander S
Dohnalkova, Alice C
Kennedy, David W
Shi, Liang
Wang, Zheming
Boyanov, Maxim I
Lai, Barry
Kemner, Kenneth M
McLean, Jeffrey S
Reed, Samantha B
Culley, David E
Bailey, Vanessa L
Simonson, Cody J
Saffarini, Daad A
Romine, Margaret F
Zachara, John M
Fredrickson, James K
author_sort Marshall, Matthew J
collection PubMed
description Modern approaches for bioremediation of radionuclide contaminated environments are based on the ability of microorganisms to effectively catalyze changes in the oxidation states of metals that in turn influence their solubility. Although microbial metal reduction has been identified as an effective means for immobilizing highly-soluble uranium(VI) complexes in situ, the biomolecular mechanisms of U(VI) reduction are not well understood. Here, we show that c-type cytochromes of a dissimilatory metal-reducing bacterium, Shewanella oneidensis MR-1, are essential for the reduction of U(VI) and formation of extracelluar UO (2) nanoparticles. In particular, the outer membrane (OM) decaheme cytochrome MtrC (metal reduction), previously implicated in Mn(IV) and Fe(III) reduction, directly transferred electrons to U(VI). Additionally, deletions of mtrC and/or omcA significantly affected the in vivo U(VI) reduction rate relative to wild-type MR-1. Similar to the wild-type, the mutants accumulated UO (2) nanoparticles extracellularly to high densities in association with an extracellular polymeric substance (EPS). In wild-type cells, this UO (2)-EPS matrix exhibited glycocalyx-like properties and contained multiple elements of the OM, polysaccharide, and heme-containing proteins. Using a novel combination of methods including synchrotron-based X-ray fluorescence microscopy and high-resolution immune-electron microscopy, we demonstrate a close association of the extracellular UO (2) nanoparticles with MtrC and OmcA (outer membrane cytochrome). This is the first study to our knowledge to directly localize the OM-associated cytochromes with EPS, which contains biogenic UO (2) nanoparticles. In the environment, such association of UO (2) nanoparticles with biopolymers may exert a strong influence on subsequent behavior including susceptibility to oxidation by O (2) or transport in soils and sediments.
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spelling pubmed-15267642006-08-16 c-Type Cytochrome-Dependent Formation of U(IV) Nanoparticles by Shewanella oneidensis Marshall, Matthew J Beliaev, Alexander S Dohnalkova, Alice C Kennedy, David W Shi, Liang Wang, Zheming Boyanov, Maxim I Lai, Barry Kemner, Kenneth M McLean, Jeffrey S Reed, Samantha B Culley, David E Bailey, Vanessa L Simonson, Cody J Saffarini, Daad A Romine, Margaret F Zachara, John M Fredrickson, James K PLoS Biol Research Article Modern approaches for bioremediation of radionuclide contaminated environments are based on the ability of microorganisms to effectively catalyze changes in the oxidation states of metals that in turn influence their solubility. Although microbial metal reduction has been identified as an effective means for immobilizing highly-soluble uranium(VI) complexes in situ, the biomolecular mechanisms of U(VI) reduction are not well understood. Here, we show that c-type cytochromes of a dissimilatory metal-reducing bacterium, Shewanella oneidensis MR-1, are essential for the reduction of U(VI) and formation of extracelluar UO (2) nanoparticles. In particular, the outer membrane (OM) decaheme cytochrome MtrC (metal reduction), previously implicated in Mn(IV) and Fe(III) reduction, directly transferred electrons to U(VI). Additionally, deletions of mtrC and/or omcA significantly affected the in vivo U(VI) reduction rate relative to wild-type MR-1. Similar to the wild-type, the mutants accumulated UO (2) nanoparticles extracellularly to high densities in association with an extracellular polymeric substance (EPS). In wild-type cells, this UO (2)-EPS matrix exhibited glycocalyx-like properties and contained multiple elements of the OM, polysaccharide, and heme-containing proteins. Using a novel combination of methods including synchrotron-based X-ray fluorescence microscopy and high-resolution immune-electron microscopy, we demonstrate a close association of the extracellular UO (2) nanoparticles with MtrC and OmcA (outer membrane cytochrome). This is the first study to our knowledge to directly localize the OM-associated cytochromes with EPS, which contains biogenic UO (2) nanoparticles. In the environment, such association of UO (2) nanoparticles with biopolymers may exert a strong influence on subsequent behavior including susceptibility to oxidation by O (2) or transport in soils and sediments. Public Library of Science 2006-08 2006-08-08 /pmc/articles/PMC1526764/ /pubmed/16875436 http://dx.doi.org/10.1371/journal.pbio.0040268 Text en Copyright: © 2006 Marshall et al. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are properly credited.
spellingShingle Research Article
Marshall, Matthew J
Beliaev, Alexander S
Dohnalkova, Alice C
Kennedy, David W
Shi, Liang
Wang, Zheming
Boyanov, Maxim I
Lai, Barry
Kemner, Kenneth M
McLean, Jeffrey S
Reed, Samantha B
Culley, David E
Bailey, Vanessa L
Simonson, Cody J
Saffarini, Daad A
Romine, Margaret F
Zachara, John M
Fredrickson, James K
c-Type Cytochrome-Dependent Formation of U(IV) Nanoparticles by Shewanella oneidensis
title c-Type Cytochrome-Dependent Formation of U(IV) Nanoparticles by Shewanella oneidensis
title_full c-Type Cytochrome-Dependent Formation of U(IV) Nanoparticles by Shewanella oneidensis
title_fullStr c-Type Cytochrome-Dependent Formation of U(IV) Nanoparticles by Shewanella oneidensis
title_full_unstemmed c-Type Cytochrome-Dependent Formation of U(IV) Nanoparticles by Shewanella oneidensis
title_short c-Type Cytochrome-Dependent Formation of U(IV) Nanoparticles by Shewanella oneidensis
title_sort c-type cytochrome-dependent formation of u(iv) nanoparticles by shewanella oneidensis
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC1526764/
https://www.ncbi.nlm.nih.gov/pubmed/16875436
http://dx.doi.org/10.1371/journal.pbio.0040268
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