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Title: Electrokinesis is a microbial behavior that requires extracellular electron transport

Abstract

Shewanella species are widespread in nature, enjoying a cosmopolitan distribution in marine,freshwater, sedimentary and soil environments (1), and have attracted considerable attention in recent years because of their ability to reduce an extensive number of different electron 3 acceptors, including the solid (oxy)hydroxides of iron and manganese, such as Fe(OH)3 and MnO2, using one or more proposed mechanisms of extracellular electron transport (EET) (2, 3). The EET ability of Shewanella species is consistent with their ability to generate electric current in microbial fuel cells in the absence of exogenous electron shuttles (4). Various strategies of extracellular electron transfer have been proposed in metal-reducing microbes, including naturally-occurring (2) or biogenic (5-7) soluble mediators that ‘shuttle’ electrons from cells to acceptors, as well as direct transfer using multiheme cytochromes located on the cell exterior (8) and transfer via conductive nanowires (9-11). S. oneidensis MR-1 features several proteins that are involved with the transport of electrons to the exterior of the cell where they play an important role with regard to the reduction of solid electron acceptors such as metal oxides. These include two outer-membrane decaheme c-type cytochromes (MtrC and OmcA), a membrane spanning protein (MtrB), and two periplasmic multi-heme c-type cytochromes (MtrAmore » and CymA). Deletion of the genes encoding any of these proteins leads to phenotypes that are greatly inhibited with regard to metal-oxide reduction and current production in microbial fuel cells (MFCs) (12, 13). The mutation of genes that code for proteins involved in the movement of cytochromes to the outer membrane also results in loss of metal-reducing phenotypes (13). The shewanellae are highly motile, by virtue of a single polar flagellum, and individual S. oneidensis MR-1 cells have been tracked swimming at speeds of up to, and sometimes over, 100 μm/sec, although the average swimming speed of cells in a population is considerably lower (14). Research has also shown that S. oneidensis MR-1 also displays chemotactic responses to several soluble electron acceptors, including Fe(III) citrate (15, 16) and that the CheA-3 histidine protein kinase is required for this chemotactic behavior to be observed (14). Strain MR-1 has 4 also been shown to be very sensitive to the presence of electron acceptors. For example, strain MR-1 ceases motility after a short time in the absence of an electron acceptor; however motility can be restored upon the re-addition of an electron acceptor. Here we present data that suggest that the shewanellae exhibit a motility response not previously reported: we call it electrokinesis. This response occurs intermittently with the cells in proximity to a solid electron acceptor, such as a manganese oxide particle or the working electrode of an electrochemical cell, and motility is observed to increase after contact. In addition to increased swimming velocities, cells occasionally pause on the solid acceptor surface, then after brief contact (up to 1 second) the cells typically swim away in the opposite direction from which they approached. Electrokinesis is not a uniform response that can be observed in all cells, although if an electron shuttle is added, all cells rapidly become motile.« less

Authors:
; ; ; ; ; ;
Publication Date:
Research Org.:
Pacific Northwest National Lab. (PNNL), Richland, WA (United States)
Sponsoring Org.:
USDOE
OSTI Identifier:
971443
Report Number(s):
PNNL-SA-70142
Journal ID: ISSN 0027-8424; PNASA6; KP1601010; TRN: US201004%%153
DOE Contract Number:  
AC05-76RL01830
Resource Type:
Journal Article
Journal Name:
Proceedings of the National Academy of Sciences of the United States of America, 107(1):326-331
Additional Journal Information:
Journal Volume: 107; Journal Issue: 1; Journal ID: ISSN 0027-8424
Country of Publication:
United States
Language:
English
Subject:
30 DIRECT ENERGY CONVERSION; BINDING ENERGY; CITRATES; CYTOCHROMES; ELECTRIC CURRENTS; ELECTROCHEMICAL CELLS; ELECTRODES; ELECTRON TRANSFER; ELECTRONS; FUEL CELLS; GENES; HISTIDINE; IRON; MANGANESE; MANGANESE OXIDES; MEMBRANES; MUTATIONS; OXIDES; PHOSPHOTRANSFERASES; PROTEINS; SOILS; STRAINS; TRANSPORT; VALENCE

Citation Formats

Harris, Howard W, El-Naggar, Mohamed Y, Bretschger, Orianna, Ward, Melissa J, Romine, Margaret F, Obraztsova, Anna, and Nealson, Kenneth H. Electrokinesis is a microbial behavior that requires extracellular electron transport. United States: N. p., 2010. Web. doi:10.1073/pnas.0907468107.
Harris, Howard W, El-Naggar, Mohamed Y, Bretschger, Orianna, Ward, Melissa J, Romine, Margaret F, Obraztsova, Anna, & Nealson, Kenneth H. Electrokinesis is a microbial behavior that requires extracellular electron transport. United States. doi:10.1073/pnas.0907468107.
Harris, Howard W, El-Naggar, Mohamed Y, Bretschger, Orianna, Ward, Melissa J, Romine, Margaret F, Obraztsova, Anna, and Nealson, Kenneth H. Tue . "Electrokinesis is a microbial behavior that requires extracellular electron transport". United States. doi:10.1073/pnas.0907468107.
@article{osti_971443,
title = {Electrokinesis is a microbial behavior that requires extracellular electron transport},
author = {Harris, Howard W and El-Naggar, Mohamed Y and Bretschger, Orianna and Ward, Melissa J and Romine, Margaret F and Obraztsova, Anna and Nealson, Kenneth H},
abstractNote = {Shewanella species are widespread in nature, enjoying a cosmopolitan distribution in marine,freshwater, sedimentary and soil environments (1), and have attracted considerable attention in recent years because of their ability to reduce an extensive number of different electron 3 acceptors, including the solid (oxy)hydroxides of iron and manganese, such as Fe(OH)3 and MnO2, using one or more proposed mechanisms of extracellular electron transport (EET) (2, 3). The EET ability of Shewanella species is consistent with their ability to generate electric current in microbial fuel cells in the absence of exogenous electron shuttles (4). Various strategies of extracellular electron transfer have been proposed in metal-reducing microbes, including naturally-occurring (2) or biogenic (5-7) soluble mediators that ‘shuttle’ electrons from cells to acceptors, as well as direct transfer using multiheme cytochromes located on the cell exterior (8) and transfer via conductive nanowires (9-11). S. oneidensis MR-1 features several proteins that are involved with the transport of electrons to the exterior of the cell where they play an important role with regard to the reduction of solid electron acceptors such as metal oxides. These include two outer-membrane decaheme c-type cytochromes (MtrC and OmcA), a membrane spanning protein (MtrB), and two periplasmic multi-heme c-type cytochromes (MtrA and CymA). Deletion of the genes encoding any of these proteins leads to phenotypes that are greatly inhibited with regard to metal-oxide reduction and current production in microbial fuel cells (MFCs) (12, 13). The mutation of genes that code for proteins involved in the movement of cytochromes to the outer membrane also results in loss of metal-reducing phenotypes (13). The shewanellae are highly motile, by virtue of a single polar flagellum, and individual S. oneidensis MR-1 cells have been tracked swimming at speeds of up to, and sometimes over, 100 μm/sec, although the average swimming speed of cells in a population is considerably lower (14). Research has also shown that S. oneidensis MR-1 also displays chemotactic responses to several soluble electron acceptors, including Fe(III) citrate (15, 16) and that the CheA-3 histidine protein kinase is required for this chemotactic behavior to be observed (14). Strain MR-1 has 4 also been shown to be very sensitive to the presence of electron acceptors. For example, strain MR-1 ceases motility after a short time in the absence of an electron acceptor; however motility can be restored upon the re-addition of an electron acceptor. Here we present data that suggest that the shewanellae exhibit a motility response not previously reported: we call it electrokinesis. This response occurs intermittently with the cells in proximity to a solid electron acceptor, such as a manganese oxide particle or the working electrode of an electrochemical cell, and motility is observed to increase after contact. In addition to increased swimming velocities, cells occasionally pause on the solid acceptor surface, then after brief contact (up to 1 second) the cells typically swim away in the opposite direction from which they approached. Electrokinesis is not a uniform response that can be observed in all cells, although if an electron shuttle is added, all cells rapidly become motile.},
doi = {10.1073/pnas.0907468107},
journal = {Proceedings of the National Academy of Sciences of the United States of America, 107(1):326-331},
issn = {0027-8424},
number = 1,
volume = 107,
place = {United States},
year = {2010},
month = {1}
}