Shewanella oneidensis MR-1 nanowires are outer membrane and periplasmic extensions of the extracellular electron transport components

Sahand Pirbadian, Sarah E. Barchinger, Kar Man Leung, Hye Suk Byun, Yamini Jangir, Rachida A. Bouhenni, Samantha B. Reed, Margaret F. Romine, Daad A. Saffarini, Liang Shi, Yuri A. Gorby, John H. Golbeck, Mohamed Y. El-Naggar

Research output: Contribution to journalArticle

261 Citations (Scopus)

Abstract

Bacterial nanowires offer an extracellular electron transport (EET) pathway for linking the respiratory chain of bacteria to external surfaces, including oxidized metals in the environment and engineered electrodes in renewable energy devices. Despite the global, environmental, and technological consequences of this biotic-abiotic interaction, the composition, physiological relevance, and electron transport mechanisms of bacterial nanowires remain unclear. We report, to our knowledge, the first in vivo observations of the formation and respiratory impact of nanowires in the model metal-reducing microbe Shewanella oneidensis MR-1. Live fluorescence measurements, immunolabeling, and quantitative gene expression analysis point to S. oneidensis MR-1 nanowires as extensions of the outer membrane and periplasm that include the multiheme cytochromes responsible for EET, rather than pilin-based structures as previously thought. These membrane extensions are associated with outer membrane vesicles, structures ubiquitous in Gram-negative bacteria, and are consistent with bacterial nanowires that mediate long-range EET by the previously proposed multistep redox hopping mechanism. Redox-functionalized membrane and vesicular extensions may represent a general microbial strategy for electron transport and energy distribution.

Original languageEnglish (US)
Pages (from-to)12883-12888
Number of pages6
JournalProceedings of the National Academy of Sciences of the United States of America
Volume111
Issue number35
DOIs
StatePublished - Sep 2 2014

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Shewanella
Nanowires
Electron Transport
Membranes
Oxidation-Reduction
Metals
Fimbriae Proteins
Renewable Energy
Periplasm
Cytochromes
Gram-Negative Bacteria
Electrodes
Fluorescence
Bacteria
Gene Expression
Equipment and Supplies

All Science Journal Classification (ASJC) codes

  • General

Cite this

Pirbadian, Sahand ; Barchinger, Sarah E. ; Leung, Kar Man ; Byun, Hye Suk ; Jangir, Yamini ; Bouhenni, Rachida A. ; Reed, Samantha B. ; Romine, Margaret F. ; Saffarini, Daad A. ; Shi, Liang ; Gorby, Yuri A. ; Golbeck, John H. ; El-Naggar, Mohamed Y. / Shewanella oneidensis MR-1 nanowires are outer membrane and periplasmic extensions of the extracellular electron transport components. In: Proceedings of the National Academy of Sciences of the United States of America. 2014 ; Vol. 111, No. 35. pp. 12883-12888.
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title = "Shewanella oneidensis MR-1 nanowires are outer membrane and periplasmic extensions of the extracellular electron transport components",
abstract = "Bacterial nanowires offer an extracellular electron transport (EET) pathway for linking the respiratory chain of bacteria to external surfaces, including oxidized metals in the environment and engineered electrodes in renewable energy devices. Despite the global, environmental, and technological consequences of this biotic-abiotic interaction, the composition, physiological relevance, and electron transport mechanisms of bacterial nanowires remain unclear. We report, to our knowledge, the first in vivo observations of the formation and respiratory impact of nanowires in the model metal-reducing microbe Shewanella oneidensis MR-1. Live fluorescence measurements, immunolabeling, and quantitative gene expression analysis point to S. oneidensis MR-1 nanowires as extensions of the outer membrane and periplasm that include the multiheme cytochromes responsible for EET, rather than pilin-based structures as previously thought. These membrane extensions are associated with outer membrane vesicles, structures ubiquitous in Gram-negative bacteria, and are consistent with bacterial nanowires that mediate long-range EET by the previously proposed multistep redox hopping mechanism. Redox-functionalized membrane and vesicular extensions may represent a general microbial strategy for electron transport and energy distribution.",
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Pirbadian, S, Barchinger, SE, Leung, KM, Byun, HS, Jangir, Y, Bouhenni, RA, Reed, SB, Romine, MF, Saffarini, DA, Shi, L, Gorby, YA, Golbeck, JH & El-Naggar, MY 2014, 'Shewanella oneidensis MR-1 nanowires are outer membrane and periplasmic extensions of the extracellular electron transport components', Proceedings of the National Academy of Sciences of the United States of America, vol. 111, no. 35, pp. 12883-12888. https://doi.org/10.1073/pnas.1410551111

Shewanella oneidensis MR-1 nanowires are outer membrane and periplasmic extensions of the extracellular electron transport components. / Pirbadian, Sahand; Barchinger, Sarah E.; Leung, Kar Man; Byun, Hye Suk; Jangir, Yamini; Bouhenni, Rachida A.; Reed, Samantha B.; Romine, Margaret F.; Saffarini, Daad A.; Shi, Liang; Gorby, Yuri A.; Golbeck, John H.; El-Naggar, Mohamed Y.

In: Proceedings of the National Academy of Sciences of the United States of America, Vol. 111, No. 35, 02.09.2014, p. 12883-12888.

Research output: Contribution to journalArticle

TY - JOUR

T1 - Shewanella oneidensis MR-1 nanowires are outer membrane and periplasmic extensions of the extracellular electron transport components

AU - Pirbadian, Sahand

AU - Barchinger, Sarah E.

AU - Leung, Kar Man

AU - Byun, Hye Suk

AU - Jangir, Yamini

AU - Bouhenni, Rachida A.

AU - Reed, Samantha B.

AU - Romine, Margaret F.

AU - Saffarini, Daad A.

AU - Shi, Liang

AU - Gorby, Yuri A.

AU - Golbeck, John H.

AU - El-Naggar, Mohamed Y.

PY - 2014/9/2

Y1 - 2014/9/2

N2 - Bacterial nanowires offer an extracellular electron transport (EET) pathway for linking the respiratory chain of bacteria to external surfaces, including oxidized metals in the environment and engineered electrodes in renewable energy devices. Despite the global, environmental, and technological consequences of this biotic-abiotic interaction, the composition, physiological relevance, and electron transport mechanisms of bacterial nanowires remain unclear. We report, to our knowledge, the first in vivo observations of the formation and respiratory impact of nanowires in the model metal-reducing microbe Shewanella oneidensis MR-1. Live fluorescence measurements, immunolabeling, and quantitative gene expression analysis point to S. oneidensis MR-1 nanowires as extensions of the outer membrane and periplasm that include the multiheme cytochromes responsible for EET, rather than pilin-based structures as previously thought. These membrane extensions are associated with outer membrane vesicles, structures ubiquitous in Gram-negative bacteria, and are consistent with bacterial nanowires that mediate long-range EET by the previously proposed multistep redox hopping mechanism. Redox-functionalized membrane and vesicular extensions may represent a general microbial strategy for electron transport and energy distribution.

AB - Bacterial nanowires offer an extracellular electron transport (EET) pathway for linking the respiratory chain of bacteria to external surfaces, including oxidized metals in the environment and engineered electrodes in renewable energy devices. Despite the global, environmental, and technological consequences of this biotic-abiotic interaction, the composition, physiological relevance, and electron transport mechanisms of bacterial nanowires remain unclear. We report, to our knowledge, the first in vivo observations of the formation and respiratory impact of nanowires in the model metal-reducing microbe Shewanella oneidensis MR-1. Live fluorescence measurements, immunolabeling, and quantitative gene expression analysis point to S. oneidensis MR-1 nanowires as extensions of the outer membrane and periplasm that include the multiheme cytochromes responsible for EET, rather than pilin-based structures as previously thought. These membrane extensions are associated with outer membrane vesicles, structures ubiquitous in Gram-negative bacteria, and are consistent with bacterial nanowires that mediate long-range EET by the previously proposed multistep redox hopping mechanism. Redox-functionalized membrane and vesicular extensions may represent a general microbial strategy for electron transport and energy distribution.

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U2 - 10.1073/pnas.1410551111

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