Soluble Iron Enhances Extracellular Electron Uptake by Shewanella oneidensis MR‐1

Abuyen, Karla; El‐Naggar, Mohamed Y.

doi:10.1002/celc.202200965

Soluble Iron Enhances Extracellular Electron Uptake by Shewanella oneidensis MR‐1

Journal Article · Wed Jan 11 00:00:00 EST 2023 · ChemElectroChem

DOI:https://doi.org/10.1002/celc.202200965· OSTI ID:1908877

^[1]; ^[2]

Molecular and Computational Biology Section Department of Biological Sciences University of Southern California Los Angeles CA 90089 USA) Website
Molecular and Computational Biology Section Department of Biological Sciences University of Southern California Los Angeles CA 90089 USA) Website, Department of Physics and Astronomy University of Southern California Los Angeles CA 90089 USA, Department of Chemistry University of Southern California Los Angeles CA 90089 USA

Abstract

Extracellular electron transfer (EET) is a process that microorganisms use to reduce or oxidize external insoluble electron acceptors or donors. Much of our mechanistic understanding of this process is derived from studies of transmembrane cytochrome complexes and extracellular redox shuttles that mediate outward EET to anodes and external electron acceptors. In contrast, there are knowledge gaps concerning the reverse process of inward EET from external electron donors to cells. Here, we describe a role for soluble iron (exogenous FeCl ₂ ) in enhancing EET from cathodes to the model EET bacterium Shewanella oneidensis MR‐1, with fumarate serving as the intracellular electron acceptor. This iron concentration‐dependent electron uptake was eradicated upon addition of an iron chelator and occurred only in the presence of fumarate reductase, confirming an electron pathway from cathodes to this periplasmic enzyme. Moreover, S. oneidensis mutants lacking specific outer membrane and periplasmic cytochromes exhibited significantly decreased current levels relative to wild‐type. These results indicate that soluble iron can function as an electron carrier to the EET machinery of S. oneidensis .

View Journal Article

Research Organization:: Univ. of Southern California, Los Angeles, CA (United States)

Sponsoring Organization:: USDOE; USDOE Office of Science (SC), Basic Energy Sciences (BES). Chemical Sciences, Geosciences & Biosciences Division (CSGB)

Grant/Contract Number:: SC0010609

OSTI ID:: 1908877

Alternate ID(s):: OSTI ID: 2420065
OSTI ID: 1924829

Journal Information:: ChemElectroChem, Journal Name: ChemElectroChem Journal Issue: 4 Vol. 10; ISSN 2196-0216

Publisher:: Wiley Blackwell (John Wiley & Sons)Copyright Statement

Country of Publication:: Germany

Language:: English

References (44)

Electronic Absorption Spectra and Redox Properties of C Type Cytochromes in Living Microbes Nakamura, Ryuhei; Ishii, Kazuyuki; Hashimoto, Kazuhito Angewandte Chemie, Vol. 121, Issue 9 https://doi.org/10.1002/ange.200804917	journal	February 2009
Flavin Redox Bifurcation as a Mechanism for Controlling the Direction of Electron Flow during Extracellular Electron Transfer Okamoto, Akihiro; Hashimoto, Kazuhito; Nealson, Kenneth H. Angewandte Chemie, Vol. 126, Issue 41 https://doi.org/10.1002/ange.201407004	journal	August 2014
Distinct Electron Conductance Regimes in Bacterial Decaheme Cytochromes Barrozo, Alexandre; El-Naggar, Mohamed Y.; Krylov, Anna I. Angewandte Chemie, Vol. 130, Issue 23 https://doi.org/10.1002/ange.201800294	journal	May 2018
Electronic Absorption Spectra and Redox Properties of C Type Cytochromes in Living Microbes Nakamura, Ryuhei; Ishii, Kazuyuki; Hashimoto, Kazuhito Angewandte Chemie International Edition, Vol. 48, Issue 9 https://doi.org/10.1002/anie.200804917	journal	January 2009
Flavin Redox Bifurcation as a Mechanism for Controlling the Direction of Electron Flow during Extracellular Electron Transfer Okamoto, Akihiro; Hashimoto, Kazuhito; Nealson, Kenneth H. Angewandte Chemie International Edition, Vol. 53, Issue 41 https://doi.org/10.1002/anie.201407004	journal	August 2014
Distinct Electron Conductance Regimes in Bacterial Decaheme Cytochromes Barrozo, Alexandre; El‐Naggar, Mohamed Y.; Krylov, Anna I. Angewandte Chemie International Edition, Vol. 57, Issue 23 https://doi.org/10.1002/anie.201800294	journal	May 2018
A Re-evaluation of Electron-Transfer Mechanisms in Microbial Electrochemistry:ShewanellaReleases Iron that Mediates Extracellular Electron Transfer Oram, Joseph; Jeuken, Lars J. C. ChemElectroChem, Vol. 3, Issue 5 https://doi.org/10.1002/celc.201500505	journal	February 2016
A review on sediment microbial fuel cells as a new source of sustainable energy and heavy metal remediation: mechanisms and future prospective: Sediment microbial fuel cells as a new source of sustainable energy Abbas, Syed Zaghum; Rafatullah, Mohd; Ismail, Norli International Journal of Energy Research, Vol. 41, Issue 9 https://doi.org/10.1002/er.3706	journal	January 2017
Identification of the gene encoding the sole physiological fumarate reductase in Shewanella oneidensis MR-1 Maier, Tamara M.; Myers, Judith M.; Myers, Charles R. Journal of Basic Microbiology, Vol. 43, Issue 4 https://doi.org/10.1002/jobm.200390034	journal	August 2003
Characterization of Shewanella oneidensis MtrC: a cell-surface decaheme cytochrome involved in respiratory electron transport to extracellular electron acceptors Hartshorne, Robert S.; Jepson, Brian N.; Clarke, Tom A. JBIC Journal of Biological Inorganic Chemistry, Vol. 12, Issue 7 https://doi.org/10.1007/s00775-007-0278-y	journal	August 2007
Electrochemical interrogations of the Mtr cytochromes from Shewanella: opening a potential window Firer-Sherwood, Mackenzie; Pulcu, Gökçe Su; Elliott, Sean J. JBIC Journal of Biological Inorganic Chemistry, Vol. 13, Issue 6 https://doi.org/10.1007/s00775-008-0398-z	journal	June 2008
Bioelectrochemical reduction of CO₂ to CH₄ via direct and indirect extracellular electron transfer by a hydrogenophilic methanogenic culture Villano, Marianna; Aulenta, Federico; Ciucci, Costanza Bioresource Technology, Vol. 101, Issue 9, p. 3085-3090 https://doi.org/10.1016/j.biortech.2009.12.077	journal	May 2010
Electrochemical growth of Acidithiobacillus ferrooxidans on a graphite electrode for obtaining a biocathode for direct electrocatalytic reduction of oxygen Carbajosa, Sofía; Malki, Moustafá; Caillard, Renaud Biosensors and Bioelectronics, Vol. 26, Issue 2 https://doi.org/10.1016/j.bios.2010.07.037	journal	October 2010
Mechanism of Electromethanogenic Reduction of CO2 by a Thermophilic Methanogen Hara, Masahiro; Onaka, Yutaka; Kobayashi, Hajime Energy Procedia, Vol. 37 https://doi.org/10.1016/j.egypro.2013.06.637	journal	January 2013
Electrochemical characterization of direct electron uptake in electrical microbially influenced corrosion of iron by the lithoautotrophic SRB Desulfopila corrodens strain IS4 Beese-Vasbender, Pascal F.; Nayak, Simantini; Erbe, Andreas Electrochimica Acta, Vol. 167 https://doi.org/10.1016/j.electacta.2015.03.184	journal	June 2015
Disentangling the roles of free and cytochrome-bound flavins in extracellular electron transport from Shewanella oneidensis MR-1 Xu, Shuai; Jangir, Yamini; El-Naggar, Mohamed Y. Electrochimica Acta, Vol. 198 https://doi.org/10.1016/j.electacta.2016.03.074	journal	April 2016
An electrochemical investigation of interfacial electron uptake by the sulfur oxidizing bacterium Thioclava electrotropha ElOx9 Karbelkar, Amruta A.; Rowe, Annette R.; El-Naggar, Mohamed Y. Electrochimica Acta, Vol. 324 https://doi.org/10.1016/j.electacta.2019.134838	journal	November 2019
A computational model for biofilm-based microbial fuel cells Picioreanu, Cristian; Head, Ian M.; Katuri, Krishna P. Water Research, Vol. 41, Issue 13 https://doi.org/10.1016/j.watres.2007.04.009	journal	July 2007
Oxidation of Fe(II) by Flavins under Anoxic Conditions Zhang, Peng; Van Cappellen, Philippe; Pi, Kunfu Environmental Science & Technology, Vol. 54, Issue 18 https://doi.org/10.1021/acs.est.0c02916	journal	August 2020
Distribution of Extracellular Flavins in a Coastal Marine Basin and Their Relationship to Redox Gradients and Microbial Community Members Monteverde, Danielle R.; Sylvan, Jason B.; Suffridge, Christopher Environmental Science & Technology, Vol. 52, Issue 21 https://doi.org/10.1021/acs.est.8b02822	journal	September 2018
Chelation of Ferrous Sulphate Solutions by Desferrioxamine B Goodwin, J. F.; Whitten, C. F. Nature, Vol. 205, Issue 4968 https://doi.org/10.1038/205281b0	journal	January 1965
Hydrogenase-independent uptake and metabolism of electrons by the archaeon Methanococcus maripaludis Lohner, Svenja T.; Deutzmann, Jörg S.; Logan, Bruce E. The ISME Journal, Vol. 8, Issue 8 https://doi.org/10.1038/ismej.2014.82	journal	May 2014
Extracellular electron transfer mechanisms between microorganisms and minerals Shi, Liang; Dong, Hailiang; Reguera, Gemma Nature Reviews Microbiology, Vol. 14, Issue 10 https://doi.org/10.1038/nrmicro.2016.93	journal	August 2016
Identification of a pathway for electron uptake in Shewanella oneidensis Rowe, Annette R.; Salimijazi, Farshid; Trutschel, Leah Communications Biology, Vol. 4, Issue 1 https://doi.org/10.1038/s42003-021-02454-x	journal	August 2021
Kinetics of trifurcated electron flow in the decaheme bacterial proteins MtrC and MtrF Jiang, Xiuyun; Burger, Bastian; Gajdos, Fruzsina Proceedings of the National Academy of Sciences, Vol. 116, Issue 9 https://doi.org/10.1073/pnas.1818003116	journal	February 2019
Electrochemical Measurement of Electron Transfer Kinetics by Shewanella oneidensis MR-1 Baron, Daniel; LaBelle, Edward; Coursolle, Dan Journal of Biological Chemistry, Vol. 284, Issue 42 https://doi.org/10.1074/jbc.M109.043455	journal	August 2009
Bioelectricity (electromicrobiology) and sustainability Nealson, Kenneth H. Microbial Biotechnology, Vol. 10, Issue 5 https://doi.org/10.1111/1751-7915.12834	journal	August 2017
Modularity of the Mtr respiratory pathway of Shewanella oneidensis strain MR-1: Modularity in S. oneidensis Coursolle, Dan; Gralnick, Jeffrey A. Molecular Microbiology https://doi.org/10.1111/j.1365-2958.2010.07266.x	journal	July 2010
A kinetic perspective on extracellular electron transfer by anode-respiring bacteria Torres, César I.; Marcus, Andrew Kato; Lee, Hyung-Sool FEMS Microbiology Reviews, Vol. 34, Issue 1 https://doi.org/10.1111/j.1574-6976.2009.00191.x	journal	January 2010
Bacterial Manganese Reduction and Growth with Manganese Oxide as the Sole Electron Acceptor Myers, C. R.; Nealson, K. H. Science, Vol. 240, Issue 4857 https://doi.org/10.1126/science.240.4857.1319	journal	June 1988
MgtE Homolog FicI Acts as a Secondary Ferrous Iron Importer in Shewanella oneidensis Strain MR-1 Bennett, Brittany D.; Redford, Kaitlyn E.; Gralnick, Jeffrey A. Applied and Environmental Microbiology, Vol. 84, Issue 6 https://doi.org/10.1128/AEM.01245-17	journal	March 2018
New Insight into Microbial Iron Oxidation as Revealed by the Proteomic Profile of an Obligate Iron-Oxidizing Chemolithoautotroph Barco, Roman A.; Emerson, David; Sylvan, Jason B. Applied and Environmental Microbiology, Vol. 81, Issue 17 https://doi.org/10.1128/AEM.01374-15	journal	June 2015
A Ferrous Iron Exporter Mediates Iron Resistance in Shewanella oneidensis MR-1 Bennett, Brittany D.; Brutinel, Evan D.; Gralnick, Jeffrey A. Applied and Environmental Microbiology, Vol. 81, Issue 22 https://doi.org/10.1128/AEM.02835-15	journal	September 2015
The Mtr Respiratory Pathway Is Essential for Reducing Flavins and Electrodes in Shewanella oneidensis Coursolle, D.; Baron, D. B.; Bond, D. R. Journal of Bacteriology, Vol. 192, Issue 2 https://doi.org/10.1128/JB.00925-09	journal	November 2009
Cultivation of an Obligate Fe(II)-Oxidizing Lithoautotrophic Bacterium Using Electrodes Summers, Zarath M.; Gralnick, Jeffrey A.; Bond, Daniel R. mBio, Vol. 4, Issue 1 https://doi.org/10.1128/mBio.00420-12	journal	January 2013
Iron Oxidation by a Fused Cytochrome-Porin Common to Diverse Iron-Oxidizing Bacteria Keffer, Jessica L.; McAllister, Sean M.; Garber, Arkadiy I. mBio, Vol. 12, Issue 4 https://doi.org/10.1128/mBio.01074-21	journal	August 2021
Tracking Electron Uptake from a Cathode into Shewanella Cells: Implications for Energy Acquisition from Solid-Substrate Electron Donors Rowe, Annette R.; Rajeev, Pournami; Jain, Abhiney mBio, Vol. 9, Issue 1 https://doi.org/10.1128/mBio.02203-17	journal	February 2018
Methane-Linked Mechanisms of Electron Uptake from Cathodes by Methanosarcina barkeri Rowe, Annette R.; Xu, Shuai; Gardel, Emily mBio, Vol. 10, Issue 2 https://doi.org/10.1128/mBio.02448-18	journal	March 2019
Sulphate-Reducing Bacteria and Anaerobic Corrosion Hamilton, W. A. Annual Review of Microbiology, Vol. 39, Issue 1 https://doi.org/10.1146/annurev.mi.39.100185.001211	journal	October 1985
Towards Electrosynthesis in Shewanella: Energetics of Reversing the Mtr Pathway for Reductive Metabolism Ross, Daniel E.; Flynn, Jeffrey M.; Baron, Daniel B. PLoS ONE, Vol. 6, Issue 2 https://doi.org/10.1371/journal.pone.0016649	journal	February 2011
Effects of Chelators (Deferoxamine, Deferiprone and Deferasirox) on the Growth ofKlebsiella PneumoniaeandAeromonas HydrophilaIsolated from Transfusion-Dependent Thalassemia Patients Chan, Godfrey Chi-Fung; Chan, Shing; Ho, Pak-Leung Hemoglobin, Vol. 33, Issue 5 https://doi.org/10.3109/03630260903211888	journal	October 2009
Reconstruction of Extracellular Respiratory Pathways for Iron(III) Reduction in Shewanella Oneidensis Strain MR-1 Coursolle, Dan; Gralnick, Jeffrey A. Frontiers in Microbiology, Vol. 3 https://doi.org/10.3389/fmicb.2012.00056	journal	January 2012
Recent Advances in the Siderophore Biology of Shewanella Liu, Lulu; Wang, Wei; Wu, Shihua Frontiers in Microbiology, Vol. 13 https://doi.org/10.3389/fmicb.2022.823758	journal	February 2022
Electron Extraction from an Extracellular Electrode by Desulfovibrio ferrophilus Strain IS5 Without Using Hydrogen as an Electron Carrier Deng, Xiao; Nakamura, Ryuhei; Hashimoto, Kazuhito Electrochemistry, Vol. 83, Issue 7 https://doi.org/10.5796/electrochemistry.83.529	journal	January 2015

Similar Records

Ultrastructure of Shewanella oneidensis MR-1 nanowires revealed by electron cryotomography

Journal Article · Sun Mar 18 20:00:00 EDT 2018 · Proceedings of the National Academy of Sciences of the United States of America · OSTI ID:1426853

Related Subjects

37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY
59 BASIC BIOLOGICAL SCIENCES
Shewanella
electron uptake
electrosynthesis
extracellular electron transfer
microbial electrochemistry

Soluble Iron Enhances Extracellular Electron Uptake by Shewanella oneidensis MR‐1

Citation Formats

References (44)

Similar Records

Related Subjects