Iodate Reduction by <i>Shewanella oneidensis</i> Does Not Involve Nitrate Reductase

Mok, Jung Kee; Toporek, Yael J.; Shin, Hyun‐Dong; Lee, Brady D.; Lee, M. Hope; DiChristina, Thomas J.

doi:10.1080/01490451.2018.1430189

Cited by 22 publications

(18 citation statements)

References 56 publications

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“…Ϫ reduction activities were not inhibited by the presence of saturating levels of the competing electron acceptor and that NO 3 Ϫ reductase-deficient deletion mutants retained wild-type IO 3 Ϫ reduction activity (33). S. oneidensis also reduces external metal oxides via EEC-mediated electron transfer either at the outside face of the outer membrane or via outer membrane extensions (i.e., nanowires) (19,35,47).…”

Section: Discussionmentioning

confidence: 97%

“…Determination of IO 3 ؊ concentrations via IO 3 ؊ -triiodide formation with I ؊ at acidic pH. The extent of IO 3 Ϫ reduction was determined using the IO 3 Ϫ -triiodide method (33,70). Culture samples were added to 96-well 500-l microtiter plates.…”

Section: Methodsmentioning

confidence: 99%

“…Previous findings for other IO 3 Ϫ -reducing microorganisms indicated that nitrate (NO 3 Ϫ ) reductase may catalyze the reduction of IO 3 Ϫ as an alternative electron acceptor (30)(31)(32). However, neither assimilatory nor dissimilatory NO 3 Ϫ reductases are required for IO 3 Ϫ reduction by S. oneidensis (33). The molecular mechanism of IO 3…”

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confidence: 96%

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Metal Reduction and Protein Secretion Genes Required for Iodate Reduction by Shewanella oneidensis

Toporek

Mok

Shin

et al. 2019

Appl Environ Microbiol

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The metal-reducing gammaproteobacterium Shewanella oneidensis reduces iodate (IO 3 Ϫ ) as an anaerobic terminal electron acceptor. Microbial IO 3 Ϫ electron transport pathways are postulated to terminate with nitrate (NO 3 Ϫ ) reductase, which reduces IO 3 Ϫ as an alternative electron acceptor. Recent studies with S. oneidensis, however, have demonstrated that NO 3Ϫ reductase is not involved in IO 3 Ϫ reduction. The main objective of the present study was to determine the metal reduction and protein secretion genes required for IO 3 Ϫ reduction by Shewanella oneidensis with lactate, formate, or H 2 as the electron donor. With all electron donors, the type I and type V protein secretion mutants retained wild-type IO 3Ϫ reduction activity, while the type II protein secretion mutant lacking the outer membrane secretin GspD was impaired in IO 3 Ϫ reduction. Deletion mutants lacking the cyclic AMP receptor protein (CRP), cytochrome maturation permease CcmB, and inner membrane-tethered c-type cytochrome CymA were impaired in IO 3Ϫ reduction with all electron donors, while deletion mutants lacking c-type cytochrome MtrA and outer membrane ␤-barrel protein MtrB of the outer membrane MtrAB module were impaired in IO 3Ϫ reduction with only lactate as an electron donor. With all electron donors, mutants lacking the c-type cytochromes OmcA and MtrC of the metalreducing extracellular electron conduit MtrCAB retained wild-type IO 3 Ϫ reduction activity. These findings indicate that IO 3 Ϫ reduction by S. oneidensis involves electron donor-dependent metal reduction and protein secretion pathway components, including the outer membrane MtrAB module and type II protein secretion of an unidentified IO 3 Ϫ reductase to the S. oneidensis outer membrane.IMPORTANCE Microbial iodate (IO 3 Ϫ ) reduction is a major component in the biogeochemical cycling of iodine and the bioremediation of iodine-contaminated environments; however, the molecular mechanism of microbial IO 3 Ϫ reduction is poorly understood. Results of the present study indicate that outer membrane (type II) protein secretion and metal reduction genes encoding the outer membrane MtrAB module of the extracellular electron conduit MtrCAB are required for IO 3 Ϫ reduction by S. oneidensis. On the other hand, the metal-reducing c-type cytochrome MtrC of the extracellular electron conduit is not required for IO 3 Ϫ reduction by S. oneidensis. These findings indicate that the IO 3 Ϫ electron transport pathway terminates with an as yet unidentified IO 3Ϫ reductase that associates with the outer membrane MtrAB module to deliver electrons extracellularly to IO 3 Ϫ .

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Section: Discussionmentioning

confidence: 97%

Section: Methodsmentioning

confidence: 99%

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Metal Reduction and Protein Secretion Genes Required for Iodate Reduction by Shewanella oneidensis

Toporek

Mok

Shin

et al. 2019

Appl Environ Microbiol

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“…IO 3 – is more thermodynamically stable in seawater than I – ; however, significant quantities of I – are detected in anaerobic environments such as anaerobic basins and oxygen minimum zones in marine environments, which potentially indicates that microbial IO 3 – reduction is a major component of the iodine biogeochemical reaction network ( Whitehead, 1984 ; Councell et al, 1997 ; Farrenkopf et al, 1997 ; Wong et al, 2002 ; Chance et al, 2007 ; Bluhm et al, 2010 ; Amachi, 2013 ; Kaplan et al, 2014 ; Fuge and Johnson, 2015 ; Guido-Garcia et al, 2015 ). Microbial IO 3 – reduction has also received recent attention as a component of alternative strategies for the remediation of waters and sediments contaminated with radioactive iodine inadvertently released to the environment ( Amachi, 2013 ; Kaplan et al, 2014 ; Riley et al, 2016 ; Mok et al, 2018 ; Toporek et al, 2019 ). The presence of environmental 129 I presents a significant risk of bioaccumulation in the human thyroid gland, as iodine is a biologically active element for humans and vertebrate animals as a constituent of the thyroid hormones, thyroxine, and triiodothyronine ( Whitehead, 1984 ; Fuge and Johnson, 2015 ).…”

Section: Introductionmentioning

confidence: 99%

“…Several IO 3 – -reducing microorganisms have been reported, which include Shewanella putrefaciens , Shewanella oneidensis , Desulfovibrio desulfuricans , Pseudomonas sp. strain SCT, and Rhizobiaceae bacterium strain DVZ35 ( Councell et al, 1997 ; Farrenkopf et al, 1997 ; Amachi et al, 2007 ; Mok et al, 2018 ; Toporek et al, 2019 ). In particular, the facultative anaerobe S. oneidensis reduces a wide range of terminal electron acceptors, which includes oxidized forms of iron, manganese, nitrogen, sulfur, uranium, plutonium, technetium, and iodine ( Farrenkopf et al, 1997 ; Venkateswaran et al, 1999 ; Neu et al, 2005 ; Newsome et al, 2014 ; Mok et al, 2018 ; Toporek et al, 2019 ).…”

Section: Introductionmentioning

confidence: 99%

Iodate Reduction by Shewanella oneidensis Requires Genes Encoding an Extracellular Dimethylsulfoxide Reductase

et al. 2022

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Microbial iodate (IO3–) reduction is a major component of the iodine biogeochemical reaction network in anaerobic marine basins and radioactive iodine-contaminated subsurface environments. Alternative iodine remediation technologies include microbial reduction of IO3– to iodide (I–) and microbial methylation of I– to volatile gases. The metal reduction pathway is required for anaerobic IO3– respiration by the gammaproteobacterium Shewanella oneidensis. However, the terminal IO3– reductase and additional enzymes involved in the S. oneidensis IO3– electron transport chain have not yet been identified. In this study, gene deletion mutants deficient in four extracellular electron conduits (EECs; ΔmtrA, ΔmtrA-ΔmtrDEF, ΔmtrA-ΔdmsEF, ΔmtrA-ΔSO4360) and DMSO reductase (ΔdmsB) of S. oneidensis were constructed and examined for anaerobic IO3– reduction activity with either 20 mM lactate or formate as an electron donor. IO3– reduction rate experiments were conducted under anaerobic conditions in defined minimal medium amended with 250 μM IO3– as anaerobic electron acceptor. Only the ΔmtrA mutant displayed a severe deficiency in IO3– reduction activity with lactate as the electron donor, which suggested that the EEC-associated decaheme cytochrome was required for lactate-dependent IO3– reduction. The ΔmtrA-ΔdmsEF triple mutant displayed a severe deficiency in IO3– reduction activity with formate as the electron donor, whereas ΔmtrA-ΔmtrDEF and ΔmtrA-ΔSO4360 retained moderate IO3– reduction activity, which suggested that the EEC-associated dimethylsulfoxide (DMSO) reductase membrane-spanning protein DmsE, but not MtrA, was required for formate-dependent IO3– reduction. Furthermore, gene deletion mutant ΔdmsB (deficient in the extracellular terminal DMSO reductase protein DmsB) and wild-type cells grown with tungsten replacing molybdenum (a required co-factor for DmsA catalytic activity) in defined growth medium were unable to reduce IO3– with either lactate or formate as the electron donor, which indicated that the DmsAB complex functions as an extracellular IO3– terminal reductase for both electron donors. Results of this study provide complementary genetic and phenotypic evidence that the extracellular DMSO reductase complex DmsAB of S. oneidensis displays broad substrate specificity and reduces IO3– as an alternate terminal electron acceptor.

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Application ofShewanellato Water Treatment Issues

Szeinbaum¹,

Toporek²,

Shin³

et al. 2019

Encyclopedia of Water

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Shewanella drives a variety of environmentally important processes, including the biogeochemical cycling of carbon, metals, metalloids, and radionuclides. The ability of Shewanella to deliver electrons extracellularly also renders this genus valuable for applications of contaminant remediation and energy generation in water treatment processes. Although the first Shewanella species was isolated and studied as a model metal‐reducing microorganism over thirty years ago, only recently has research focused on employing Shewanella to drive water treatment processes. This article examines current and prospective applications of Shewanella to water treatment issues, highlighting biochemical details associated with each technology. The technologies include the remediation of metal‐contaminated environments, the generation of electricity from wastewater streams, the removal of hazardous contaminants under anaerobic conditions, and precious metal recovery in combination with formation of novel biocatalysts.

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Iodate Reduction by Shewanella oneidensis Does Not Involve Nitrate Reductase

Cited by 22 publications

References 56 publications

Metal Reduction and Protein Secretion Genes Required for Iodate Reduction by Shewanella oneidensis

Metal Reduction and Protein Secretion Genes Required for Iodate Reduction by Shewanella oneidensis

Iodate Reduction by Shewanella oneidensis Requires Genes Encoding an Extracellular Dimethylsulfoxide Reductase

Application ofShewanellato Water Treatment Issues

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