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

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          Abstract

          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.

          Abstract

          Microorganisms that catalyze changes in oxidation states of metals can be used to decontaminate environments of radionuclides. Here, c-type cytochromes on the outer membrane of a dissimilatory metal reducing bacterium are shown to be essential for the reduction of uranium(VI).

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          Most cited references45

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          Microbial reduction of uranium

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            Methods for generating precise deletions and insertions in the genome of wild-type Escherichia coli: application to open reading frame characterization.

            We have developed a new system of chromosomal mutagenesis in order to study the functions of uncharacterized open reading frames (ORFs) in wild-type Escherichia coli. Because of the operon structure of this organism, traditional methods such as insertional mutagenesis run the risk of introducing polar effects on downstream genes or creating secondary mutations elsewhere in the genome. Our system uses crossover PCR to create in-frame, tagged deletions in chromosomal DNA. These deletions are placed in the E. coli chromosome by using plasmid pKO3, a gene replacement vector that contains a temperature-sensitive origin of replication and markers for positive and negative selection for chromosomal integration and excision. Using kanamycin resistance (Kn(r)) insertional alleles of the essential genes pepM and rpsB cloned into the replacement vector, we calibrated the system for the expected results when essential genes are deleted. Two poorly understood genes, hdeA and yjbJ, encoding highly abundant proteins were selected as targets for this approach. When the system was used to replace chromosomal hdeA with insertional alleles, we observed vastly different results that were dependent on the exact nature of the insertions. When a Kn(r) gene was inserted into hdeA at two different locations and orientations, both essential and nonessential phenotypes were seen. Using PCR-generated deletions, we were able to make in-frame deletion strains of both hdeA and yjbJ. The two genes proved to be nonessential in both rich and glucose-minimal media. In competition experiments using isogenic strains, the strain with the insertional allele of yjbJ showed growth rates different from those of the strain with the deletion allele of yjbJ. These results illustrate that in-frame, unmarked deletions are among the most reliable types of mutations available for wild-type E. coli. Because these strains are isogenic with the exception of their deleted ORFs, they may be used in competition with one another to reveal phenotypes not apparent when cultured singly.
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              Genome of Geobacter sulfurreducens: metal reduction in subsurface environments.

              The complete genome sequence of Geobacter sulfurreducens, a delta-proteobacterium, reveals unsuspected capabilities, including evidence of aerobic metabolism, one-carbon and complex carbon metabolism, motility, and chemotactic behavior. These characteristics, coupled with the possession of many two-component sensors and many c-type cytochromes, reveal an ability to create alternative, redundant, electron transport networks and offer insights into the process of metal ion reduction in subsurface environments. As well as playing roles in the global cycling of metals and carbon, this organism clearly has the potential for use in bioremediation of radioactive metals and in the generation of electricity.
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                Author and article information

                Contributors
                Role: Academic Editor
                Journal
                PLoS Biol
                pbio
                PLoS Biology
                Public Library of Science (San Francisco, USA )
                1544-9173
                1545-7885
                August 2006
                8 August 2006
                : 4
                : 8
                : e268
                Affiliations
                [1] 1Biological Sciences Division, Pacific Northwest National Laboratory, Richland, Washington, United States of America
                [2] 2Chemical Sciences Division, Pacific Northwest National Laboratory, Richland, Washington, United States of America
                [3] 3Biosciences Division, Argonne National Laboratory, Argonne, Illinois, United States of America
                [4] 4Advanced Photon Source, Argonne National Laboratory, Argonne, Illinois, United States of America
                [5] 5Department of Biological Sciences, University of Wisconsin, Milwaukee, Wisconsin, United States of America
                The Institute for Genomic Research United States of America
                Article
                10.1371/journal.pbio.0040268
                1526764
                16875436
                fd3c72b1-9182-4e0b-8273-3c09091383ed
                Copyright: © 2006 Marshall et al. 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 credited.
                History
                : 8 February 2006
                : 12 June 2006
                Categories
                Research Article
                Microbiology
                Eubacteria

                Life sciences
                Life sciences

                Comments

                added an editorial note to Shewanella

                Shewanella can reduce Uranium ions for its respiration, precipitating U(IV) nanoparticles, offering obvious technological advantages. Here Marshall et al explore the roles of outer membrane cytochromes and the extracellular polymeric substance in this process.

                2016-03-21 14:07 UTC
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