Metal Reduction and Protein Secretion Genes Required for Iodate Reduction by Shewanella oneidensis
Abstract
The metal-reducing gammaproteobacteriumShewanella oneidensisreduces iodate (IO3-) as an anaerobic terminal electron acceptor. Microbial IO3-electron transport pathways are postulated to terminate with nitrate (NO3-) reductase, which reduces IO3-as an alternative electron acceptor. Recent studies withS. oneidensis, however, have demonstrated that NO3-reductase is not involved in IO3-reduction. The main objective of the present study was to determine the metal reduction and protein secretion genes required for IO3-reduction byShewanella oneidensiswith lactate, formate, or H2as the electron donor. With all electron donors, the type I and type V protein secretion mutants retained wild-type IO3-reduction activity, while the type II protein secretion mutant lacking the outer membrane secretin GspD was impaired in IO3-reduction. Deletion mutants lacking the cyclic AMP receptor protein (CRP), cytochrome maturation permease CcmB, and inner membrane-tetheredc-type cytochrome CymA were impaired in IO3-reduction with all electron donors, while deletion mutants lackingc-type cytochrome MtrA and outer membrane β-barrel protein MtrB of the outer membrane MtrAB module were impaired in IO3-reduction with only lactate as an electron donor. With all electron donors, mutants lacking thec-type cytochromes OmcA and MtrC of the metal-reducing extracellular electron conduit MtrCAB retained wild-type IO3-reduction activity. These findings indicate that IO3-reduction byS. oneidensisinvolves electron donor-dependent metal reduction and protein secretion pathwaymore »
- Authors:
-
[1];
- Georgia Inst. of Technology, Atlanta, GA (United States)
- Pacific Northwest National Lab. (PNNL), Richland, WA (United States)
- Savannah River National Lab., Aiken, SC (United States)
- Goethe Univ., Frankfurt am Main (Germany)
- Publication Date:
- Research Org.:
- Pacific Northwest National Lab. (PNNL), Richland, WA (United States)
- Sponsoring Org.:
- USDOE
- OSTI Identifier:
- 1501527
- Report Number(s):
- PNNL-SA-137826
Journal ID: ISSN 0099-2240
- Grant/Contract Number:
- AC05-76RL01830
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Applied and Environmental Microbiology
- Additional Journal Information:
- Journal Volume: 85; Journal Issue: 3; Journal ID: ISSN 0099-2240
- Publisher:
- American Society for Microbiology
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; 54 ENVIRONMENTAL SCIENCES; Shewanella oneidensis; iodate; iodine; metals; reduction
Citation Formats
Toporek, Yael J., Mok, Jung Kee, Shin, Hyun Dong, Lee, Brady D., Lee, M. Hope, DiChristina, Thomas J., and Müller, Volker. Metal Reduction and Protein Secretion Genes Required for Iodate Reduction by Shewanella oneidensis. United States: N. p., 2019.
Web. doi:10.1128/AEM.02115-18.
Toporek, Yael J., Mok, Jung Kee, Shin, Hyun Dong, Lee, Brady D., Lee, M. Hope, DiChristina, Thomas J., & Müller, Volker. Metal Reduction and Protein Secretion Genes Required for Iodate Reduction by Shewanella oneidensis. United States. https://doi.org/10.1128/AEM.02115-18
Toporek, Yael J., Mok, Jung Kee, Shin, Hyun Dong, Lee, Brady D., Lee, M. Hope, DiChristina, Thomas J., and Müller, Volker. Wed .
"Metal Reduction and Protein Secretion Genes Required for Iodate Reduction by Shewanella oneidensis". United States. https://doi.org/10.1128/AEM.02115-18. https://www.osti.gov/servlets/purl/1501527.
@article{osti_1501527,
title = {Metal Reduction and Protein Secretion Genes Required for Iodate Reduction by Shewanella oneidensis},
author = {Toporek, Yael J. and Mok, Jung Kee and Shin, Hyun Dong and Lee, Brady D. and Lee, M. Hope and DiChristina, Thomas J. and Müller, Volker},
abstractNote = {The metal-reducing gammaproteobacteriumShewanella oneidensisreduces iodate (IO3-) as an anaerobic terminal electron acceptor. Microbial IO3-electron transport pathways are postulated to terminate with nitrate (NO3-) reductase, which reduces IO3-as an alternative electron acceptor. Recent studies withS. oneidensis, however, have demonstrated that NO3-reductase is not involved in IO3-reduction. The main objective of the present study was to determine the metal reduction and protein secretion genes required for IO3-reduction byShewanella oneidensiswith lactate, formate, or H2as the electron donor. With all electron donors, the type I and type V protein secretion mutants retained wild-type IO3-reduction activity, while the type II protein secretion mutant lacking the outer membrane secretin GspD was impaired in IO3-reduction. Deletion mutants lacking the cyclic AMP receptor protein (CRP), cytochrome maturation permease CcmB, and inner membrane-tetheredc-type cytochrome CymA were impaired in IO3-reduction with all electron donors, while deletion mutants lackingc-type cytochrome MtrA and outer membrane β-barrel protein MtrB of the outer membrane MtrAB module were impaired in IO3-reduction with only lactate as an electron donor. With all electron donors, mutants lacking thec-type cytochromes OmcA and MtrC of the metal-reducing extracellular electron conduit MtrCAB retained wild-type IO3-reduction activity. These findings indicate that IO3-reduction byS. oneidensisinvolves electron donor-dependent metal reduction and protein secretion pathway components, including the outer membrane MtrAB module and type II protein secretion of an unidentified IO3-reductase to theS. oneidensisouter membrane.},
doi = {10.1128/AEM.02115-18},
journal = {Applied and Environmental Microbiology},
number = 3,
volume = 85,
place = {United States},
year = {Wed Jan 23 00:00:00 EST 2019},
month = {Wed Jan 23 00:00:00 EST 2019}
}
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Works referenced in this record:
Structural modeling of an outer membrane electron conduit from a metal-reducing bacterium suggests electron transfer via periplasmic redox partners
journal, April 2018
- Edwards, Marcus J.; White, Gaye F.; Lockwood, Colin W.
- Journal of Biological Chemistry, Vol. 293, Issue 21
Volatile biogenic halocarbons in the northwest Atlantic
journal, March 1993
- Moore, R. M.; Tokarczyk, R.
- Global Biogeochemical Cycles, Vol. 7, Issue 1
Reduction of iodate in seawater during Arabian Sea shipboard incubations and in laboratory cultures of the marine bacterium Shewanella putrefaciens strain MR-4
journal, July 1997
- Farrenkopf, Anna M.; Dollhopf, Michael E.; Chadhain, Sinéad Ní
- Marine Chemistry, Vol. 57, Issue 3-4
Shewanella oneidensis MR-1 mutants selected for their inability to produce soluble organic-Fe(III) complexes are unable to respire Fe(III) as anaerobic electron acceptor: Soluble Fe(III) production by Shewanella oneidensis
journal, January 2010
- Jones, Morris E.; Fennessey, Christine M.; DiChristina, Thomas J.
- Environmental Microbiology, Vol. 12, Issue 4
The biogeochemistry and bioremediation of uranium and other priority radionuclides
journal, January 2014
- Newsome, Laura; Morris, Katherine; Lloyd, Jonathan R.
- Chemical Geology, Vol. 363
Bioreduction of iodate in sediment microcosms
journal, November 2015
- Guido-Garcia, Fabiola; Law, Gareth T. W.; Lloyd, Jonathan R.
- Mineralogical Magazine, Vol. 79, Issue 6
Dissimilatory Fe(III) and Mn(IV) Reduction by Shewanella putrefaciens Requires ferE, a Homolog of the pulE (gspE) Type II Protein Secretion Gene
journal, January 2002
- DiChristina, T. J.; Moore, C. M.; Haller, C. A.
- Journal of Bacteriology, Vol. 184, Issue 1
Involvement of Cyclic AMP (cAMP) and cAMP Receptor Protein in Anaerobic Respiration of Shewanella oneidensis
journal, June 2003
- Saffarini, D. A.; Schultz, R.; Beliaev, A.
- Journal of Bacteriology, Vol. 185, Issue 12
Rapid electron exchange between surface-exposed bacterial cytochromes and Fe(III) minerals
journal, March 2013
- White, G. F.; Shi, Z.; Shi, L.
- Proceedings of the National Academy of Sciences, Vol. 110, Issue 16
Anaerobic Respiration of Elemental Sulfur and Thiosulfate by Shewanella oneidensis MR-1 Requires psrA, a Homolog of the phsA Gene of Salmonella enterica Serovar Typhimurium LT2
journal, June 2009
- Burns, J. L.; DiChristina, T. J.
- Applied and Environmental Microbiology, Vol. 75, Issue 16
Four new derivatives of the broad-host-range cloning vector pBBR1MCS, carrying different antibiotic-resistance cassettes
journal, December 1995
- Kovach, Michael E.; Elzer, Philip H.; Steven Hill, D.
- Gene, Vol. 166, Issue 1
Iodine-129 in Seawater Offshore Fukushima: Distribution, Inorganic Speciation, Sources, and Budget
journal, March 2013
- Hou, Xiaolin; Povinec, Pavel P.; Zhang, Luyuan
- Environmental Science & Technology, Vol. 47, Issue 7
Phenazines and Other Redox-Active Antibiotics Promote Microbial Mineral Reduction
journal, February 2004
- Hernandez, M. E.; Kappler, A.; Newman, D. K.
- Applied and Environmental Microbiology, Vol. 70, Issue 2
Electron transport and protein secretion pathways involved in Mn(III) reduction by S hewanella oneidensis : Mn(III) reduction by
journal, May 2014
- Szeinbaum, Nadia; Burns, Justin L.; DiChristina, Thomas J.
- Environmental Microbiology Reports, Vol. 6, Issue 5
Protective Role of tolC in Efflux of the Electron Shuttle Anthraquinone-2,6-Disulfonate
journal, March 2002
- Shyu, J. B. H.; Lies, D. P.; Newman, D. K.
- Journal of Bacteriology, Vol. 184, Issue 6
Formation of iodide-iodine in the ocean
journal, November 1969
- Tsunogai, S.; Sase, T.
- Deep Sea Research and Oceanographic Abstracts, Vol. 16, Issue 5
Maintenance of broad-host-range incompatibility group P and group Q plasmids and transposition of Tn5 in Bartonella henselae following conjugal plasmid transfer from Escherichia coli.
journal, January 1997
- Dehio, C.; Meyer, M.
- Journal of Bacteriology, Vol. 179, Issue 2
Spectrophotometric Determination of Periodate, Iodate and Bromate Mixtures Based on Their Reaction with Iodide.
journal, January 2001
- Afkhami, Abbas; Madrakian, Tayyebeh; Zarei, Ali Reza
- Analytical Sciences, Vol. 17, Issue 10
Thiol-Based Redox Switches and Gene Regulation
journal, March 2011
- Antelmann, Haike; Helmann, John D.
- Antioxidants & Redox Signaling, Vol. 14, Issue 6
Polyphasic taxonomy of the genus Shewanella and description of Shewanella oneidensis sp. nov.
journal, April 1999
- Venkateswaran, K.; Moser, D. P.; Dollhopf, M. E.
- International Journal of Systematic Bacteriology, Vol. 49, Issue 2
Mtr extracellular electron-transfer pathways in Fe(III)-reducing or Fe(II)-oxidizing bacteria: a genomic perspective
journal, November 2012
- Shi, Liang; Rosso, Kevin M.; Zachara, John M.
- Biochemical Society Transactions, Vol. 40, Issue 6
Siderophores Are Not Involved in Fe(III) Solubilization during Anaerobic Fe(III) Respiration by Shewanella oneidensis MR-1
journal, February 2010
- Fennessey, C. M.; Jones, M. E.; Taillefert, M.
- Applied and Environmental Microbiology, Vol. 76, Issue 8
Overlapping role of the outer membrane cytochromes of Shewanella oneidensis MR-1 in the reduction of manganese(IV) oxide
journal, July 2003
- Myers, J. M.; Myers, C. R.
- Letters in Applied Microbiology, Vol. 37, Issue 1
Reduction of iodate to iodide by cold water diatom cultures
journal, April 2007
- Chance, Rosie; Malin, Gill; Jickells, Tim
- Marine Chemistry, Vol. 105, Issue 1-2
Shewanella putrefaciens produces an Fe(III)-solubilizing organic ligand during anaerobic respiration on insoluble Fe(III) oxides
journal, November 2007
- Taillefert, Martial; Beckler, Jordon S.; Carey, Elizabeth
- Journal of Inorganic Biochemistry, Vol. 101, Issue 11-12
Distribution of iodide and iodate in the Atlantic sector of the southern ocean during austral summer
journal, December 2011
- Bluhm, K.; Croot, P. L.; Huhn, O.
- Deep Sea Research Part II: Topical Studies in Oceanography, Vol. 58, Issue 25-26
Microbial Mn(IV) reduction requires an initial one-electron reductive solubilization step
journal, December 2012
- Lin, Hui; Szeinbaum, Nadia H.; DiChristina, Thomas J.
- Geochimica et Cosmochimica Acta, Vol. 99
Outer Membrane-Associated Serine Protease Involved in Adhesion of Shewanella oneidensis to Fe(III) Oxides
journal, January 2010
- Burns, Justin L.; Ginn, Brian R.; Bates, David J.
- Environmental Science & Technology, Vol. 44, Issue 1
Shewanella secretes flavins that mediate extracellular electron transfer
journal, March 2008
- Marsili, E.; Baron, D. B.; Shikhare, I. D.
- Proceedings of the National Academy of Sciences, Vol. 105, Issue 10
Isolation of a High-Affinity Functional Protein Complex between OmcA and MtrC: Two Outer Membrane Decaheme c-Type Cytochromes of Shewanella oneidensis MR-1
journal, June 2006
- Shi, L.; Chen, B.; Wang, Z.
- Journal of Bacteriology, Vol. 188, Issue 13
Molecular Underpinnings of Fe(III) Oxide Reduction by Shewanella Oneidensis MR-1
journal, January 2012
- Shi, Liang; Rosso, Kevin M.; Clarke, Tomas A.
- Frontiers in Microbiology, Vol. 3
Direct Involvement of Type II Secretion System in Extracellular Translocation of Shewanella oneidensis Outer Membrane Cytochromes MtrC and OmcA
journal, May 2008
- Shi, L.; Deng, S.; Marshall, M. J.
- Journal of Bacteriology, Vol. 190, Issue 15
Extracellular electron transfer through microbial reduction of solid-phase humic substances
journal, May 2010
- Roden, Eric E.; Kappler, Andreas; Bauer, Iris
- Nature Geoscience, Vol. 3, Issue 6
c-Type Cytochrome-Dependent Formation of U(IV) Nanoparticles by Shewanella oneidensis
journal, August 2006
- Marshall, Matthew J.; Beliaev, Alexander S.; Dohnalkova, Alice C.
- PLoS Biology, Vol. 4, Issue 8
Radioiodine Biogeochemistry and Prevalence in Groundwater
journal, August 2014
- Kaplan, D. I.; Denham, M. E.; Zhang, S.
- Critical Reviews in Environmental Science and Technology, Vol. 44, Issue 20
Transformation of iodate to iodide in marine phytoplankton driven by cell senescence
journal, October 2010
- Bluhm, K.; Croot, P.; Wuttig, K.
- Aquatic Biology, Vol. 11, Issue 1
Periplasmic Electron Transfer via the c-Type Cytochromes MtrA and FccA of Shewanella oneidensis MR-1
journal, October 2009
- Schuetz, B.; Schicklberger, M.; Kuermann, J.
- Applied and Environmental Microbiology, Vol. 75, Issue 24
One-step preparation of competent Escherichia coli: transformation and storage of bacterial cells in the same solution.
journal, April 1989
- Chung, C. T.; Niemela, S. L.; Miller, R. H.
- Proceedings of the National Academy of Sciences, Vol. 86, Issue 7
Determination of iodide, iodate and organo-iodine in waters with a new total organic iodine measurement approach
journal, November 2013
- Gong, Tingting; Zhang, Xiangru
- Water Research, Vol. 47, Issue 17
Iodate Reduction by Shewanella oneidensis Does Not Involve Nitrate Reductase
journal, March 2018
- Mok, Jung Kee; Toporek, Yael J.; Shin, Hyun-Dong
- Geomicrobiology Journal, Vol. 35, Issue 7
Cloning and sequence of cymA, a gene encoding a tetraheme cytochrome c required for reduction of iron(III), fumarate, and nitrate by Shewanella putrefaciens MR-1.
journal, February 1997
- Myers, C. R.; Myers, J. M.
- Journal of Bacteriology, Vol. 179, Issue 4
Roles of Thiol-Redox Pathways in Bacteria
journal, October 2001
- Ritz, Daniel; Beckwith, Jon
- Annual Review of Microbiology, Vol. 55, Issue 1
The ‘porin-cytochrome’ model for microbe-to-mineral electron transfer: Microbe-to-mineral electron transfer
journal, May 2012
- Richardson, David J.; Butt, Julea N.; Fredrickson, Jim K.
- Molecular Microbiology, Vol. 85, Issue 2
The distribution and transformations of iodine in the environment
journal, January 1984
- Whitehead, D. C.
- Environment International, Vol. 10, Issue 4
Characterization of Protein-Protein Interactions Involved in Iron Reduction by Shewanella oneidensis MR-1
journal, August 2007
- Ross, D. E.; Ruebush, S. S.; Brantley, S. L.
- Applied and Environmental Microbiology, Vol. 73, Issue 18
Iodate and nitrate transformation by Agrobacterium/Rhizobium related strain DVZ35 isolated from contaminated Hanford groundwater
journal, May 2018
- Lee, Brady D.; Ellis, Joshua T.; Dodwell, Alex
- Journal of Hazardous Materials, Vol. 350
Type II secretion: a protein secretion system for all seasons
journal, December 2005
- Cianciotto, Nicholas P.
- Trends in Microbiology, Vol. 13, Issue 12
A Conserved Histidine in Cytochrome c Maturation Permease CcmB of Shewanella putrefaciens Is Required for Anaerobic Growth below a Threshold Standard Redox Potential
journal, December 2006
- Dale, J. R.; Wade, R.; DiChristina, T. J.
- Journal of Bacteriology, Vol. 189, Issue 3
Speciation of dissolved iodine: integrating nitrate uptake over time in the oceans
journal, January 2001
- Wong, George T. F.; Hung, Chin-Chang
- Continental Shelf Research, Vol. 21, Issue 2
Structural insights into the Type II secretion nanomachine
journal, April 2012
- McLaughlin, Lorraine S.; Haft, Rembrandt JF; Forest, Katrina T.
- Current Opinion in Structural Biology, Vol. 22, Issue 2
The transformation of iodate to iodide in marine phytoplankton cultures
journal, January 2002
- Wong, Gtf; Piumsomboon, Au; Dunstan, Wm
- Marine Ecology Progress Series, Vol. 237
A functional description of CymA, an electron-transfer hub supporting anaerobic respiratory flexibility in Shewanella
journal, May 2012
- Marritt, Sophie J.; Lowe, Thomas G.; Bye, Jordan
- Biochemical Journal, Vol. 444, Issue 3
Geochemical controls of iodine uptake and transport in Savannah River Site subsurface sediments
journal, June 2014
- Emerson, Hilary P.; Xu, Chen; Ho, Yi-Fang
- Applied Geochemistry, Vol. 45
Bacterial Manganese Reduction and Growth with Manganese Oxide as the Sole Electron Acceptor
journal, June 1988
- Myers, C. R.; Nealson, K. H.
- Science, Vol. 240, Issue 4857
Kinetics of Reduction of Fe(III) Complexes by Outer Membrane Cytochromes MtrC and OmcA of Shewanella oneidensis MR-1
journal, September 2008
- Wang, Z.; Liu, C.; Wang, X.
- Applied and Environmental Microbiology, Vol. 74, Issue 21
Nuclear Data Sheets for A = 129
journal, September 2014
- Timar, Janos; Elekes, Zoltan; Singh, Balraj
- Nuclear Data Sheets, Vol. 121
Development of a proteoliposome model to probe transmembrane electron-transfer reactions
journal, November 2012
- White, Gaye F.; Shi, Zhi; Shi, Liang
- Biochemical Society Transactions, Vol. 40, Issue 6
Dissimilatory Reduction of Extracellular Electron Acceptors in Anaerobic Respiration
journal, December 2011
- Richter, Katrin; Schicklberger, Marcus; Gescher, Johannes
- Applied and Environmental Microbiology, Vol. 78, Issue 4
Speciation of 129 I and 127 I in Seawater and Implications for Sources and Transport Pathways in the North Sea
journal, September 2007
- Hou, Xiaolin; Aldahan, Ala; Nielsen, Sven P.
- Environmental Science & Technology, Vol. 41, Issue 17
The Mtr Respiratory Pathway Is Essential for Reducing Flavins and Electrodes in Shewanella oneidensis
journal, November 2009
- Coursolle, D.; Baron, D. B.; Bond, D. R.
- Journal of Bacteriology, Vol. 192, Issue 2
Electrically conductive bacterial nanowires produced by Shewanella oneidensis strain MR-1 and other microorganisms
journal, July 2006
- Gorby, Y. A.; Yanina, S.; McLean, J. S.
- Proceedings of the National Academy of Sciences, Vol. 103, Issue 30
Localization of cytochromes to the outer membrane of anaerobically grown Shewanella putrefaciens MR-1.
journal, June 1992
- Myers, C. R.; Myers, J. M.
- Journal of Bacteriology, Vol. 174, Issue 11
Modularity of the Mtr respiratory pathway of Shewanella oneidensis strain MR-1: Modularity in S. oneidensis
journal, July 2010
- Coursolle, Dan; Gralnick, Jeffrey A.
- Molecular Microbiology
Identification of a molecular signature unique to metal-reducing Gammaproteobacteria
journal, November 2013
- Wee, Seng K.; Burns, Justin L.; DiChristina, Thomas J.
- FEMS Microbiology Letters, Vol. 350, Issue 1
Dissimilatory Iodate Reduction by Marine Pseudomonas sp. Strain SCT
journal, July 2007
- Amachi, S.; Kawaguchi, N.; Muramatsu, Y.
- Applied and Environmental Microbiology, Vol. 73, Issue 18
Regulation and Maturation of the Shewanella oneidensis Sulfite Reductase SirA
journal, January 2020
- Brockman, Kenneth L.; Shirodkar, Sheetal; Croft, Trevor J.
- Scientific Reports, Vol. 10, Issue 1
The Ethanologenic Bacterium Zymomonas mobilis Divides Asymmetrically and Exhibits Heterogeneity in DNA Content
journal, February 2021
- Fuchino, Katsuya; Chan, Helena; Hwang, Ling Chin
- Applied and Environmental Microbiology, Vol. 87, Issue 6
Nuclear Data Sheets for A = 129
journal, July 1983
- Hashizume, A.; Tendow, Y.; Ohshima, M.
- Nuclear Data Sheets, Vol. 39, Issue 3