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...
| Main Authors: | , , , , , , , , , , , , , , , , , |
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| Format: | Article |
| Language: | English |
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Public Library of Science (PLoS)
2006-09-01
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| Series: | PLoS Biology |
| Online Access: | http://europepmc.org/articles/PMC1526764?pdf=render |
| _version_ | 1818655621509021696 |
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| author | Matthew J Marshall Alexander S Beliaev Alice C Dohnalkova David W Kennedy Liang Shi Zheming Wang Maxim I Boyanov Barry Lai Kenneth M Kemner Jeffrey S McLean Samantha B Reed David E Culley Vanessa L Bailey Cody J Simonson Daad A Saffarini Margaret F Romine John M Zachara James K Fredrickson |
| author_facet | Matthew J Marshall Alexander S Beliaev Alice C Dohnalkova David W Kennedy Liang Shi Zheming Wang Maxim I Boyanov Barry Lai Kenneth M Kemner Jeffrey S McLean Samantha B Reed David E Culley Vanessa L Bailey Cody J Simonson Daad A Saffarini Margaret F Romine John M Zachara James K Fredrickson |
| author_sort | Matthew J Marshall |
| collection | DOAJ |
| 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 extracellular 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. |
| first_indexed | 2024-12-17T03:12:36Z |
| format | Article |
| id | doaj.art-3410be2a22bb45439a9c40ea29bdd10e |
| institution | Directory Open Access Journal |
| issn | 1544-9173 1545-7885 |
| language | English |
| last_indexed | 2024-12-17T03:12:36Z |
| publishDate | 2006-09-01 |
| publisher | Public Library of Science (PLoS) |
| record_format | Article |
| series | PLoS Biology |
| spelling | doaj.art-3410be2a22bb45439a9c40ea29bdd10e2022-12-21T22:05:47ZengPublic Library of Science (PLoS)PLoS Biology1544-91731545-78852006-09-0149e26810.1371/journal.pbio.0040268c-Type cytochrome-dependent formation of U(IV) nanoparticles by Shewanella oneidensis.Matthew J MarshallAlexander S BeliaevAlice C DohnalkovaDavid W KennedyLiang ShiZheming WangMaxim I BoyanovBarry LaiKenneth M KemnerJeffrey S McLeanSamantha B ReedDavid E CulleyVanessa L BaileyCody J SimonsonDaad A SaffariniMargaret F RomineJohn M ZacharaJames K FredricksonModern 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 extracellular 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.http://europepmc.org/articles/PMC1526764?pdf=render |
| spellingShingle | Matthew J Marshall Alexander S Beliaev Alice C Dohnalkova David W Kennedy Liang Shi Zheming Wang Maxim I Boyanov Barry Lai Kenneth M Kemner Jeffrey S McLean Samantha B Reed David E Culley Vanessa L Bailey Cody J Simonson Daad A Saffarini Margaret F Romine John M Zachara James K Fredrickson c-Type cytochrome-dependent formation of U(IV) nanoparticles by Shewanella oneidensis. PLoS Biology |
| 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 |
| url | http://europepmc.org/articles/PMC1526764?pdf=render |
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