Secretion of Flavins by
            <i>Shewanella</i>
            Species and Their Role in Extracellular Electron Transfer

Canstein, Harald von; Ogawa, Jun; Shimizu, Sakayu; Lloyd, Jonathan R.

doi:10.1128/aem.01387-07

Cited by 790 publications

(703 citation statements)

References 32 publications

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“…6). Although flavin adenine mononcleotide (FMN) has been detected in supernatants of different Shewanella species [23], we did not detect it in our experiments, perhaps due to differences in experimental design. Surprisingly, the levels of riboflavins in supernatants of Dflg, Dmsh, DpilM-Q, DmtrC /DomcA were similar to wild type levels (Fig.…”

Section: Role Of Riboflavins In Extracellular Electron Transfer In Picontrasting

confidence: 47%

“…Recently, flavins were proposed to be soluble mediators in extracellular electron transfer to Fe(III) oxides and to anodes of MFCs [22,23]. To determine if these mediators contributed to the differences in current output by wild type and mutant strains, we measured flavin levels in culture supernatants at the end of the MFC experiments (210 h).…”

Section: Role Of Riboflavins In Extracellular Electron Transfer In Pimentioning

confidence: 99%

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The Role of Shewanella oneidensis MR‐1 Outer Surface Structures in Extracellular Electron Transfer

et al. 2010

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The ability of the metal reducer Shewanella oneidensis MR-1 to generate electricity in microbial fuel cells (MFCs) depends on the activity of a predicted type IV prepilin peptidase; PilD. Analysis of an S. oneidensis MR-1 pilD mutant indicated that it was deficient in pili production (Msh and type IV) and type II secretion (T2S). The requirement for T2S in metal reduction has been previously identified, but the role of pili remains largely unexplored. To define the role of type IV or Msh pili in electron transfer, mutants that lack one or both pilus biogenesis systems were generated and analyzed; a mutant that lacked flagella was also constructed and tested. All mutants were able to reduce insoluble Fe(III) and to generate current in MFCs, in contrast to the T2S mutant that is deficient in both processes. Our results show that loss of metal reduction in a PilD mutant is due to a T2S deficiency, and therefore the absence of c cytochromes from the outer surface of MR-1 cells, and not the loss of pili or flagella. Furthermore, MR-1 mutants deficient in type IV pili or flagella generated more current than the wild type, even though extracellular riboflavin levels were similar in all strains. This enhanced current generating ability is in contrast to a mutant that lacks the outer membrane c cytochromes, MtrC and OmcA. This mutant generated significantly less current than the wild type in an MFC and was unable to reduce Fe(III). These results indicated that although nanofilaments and soluble mediators may play a role in electron transfer, surface exposure of outer membrane c cytochromes was the determining factor in extracellular electron transfer in S. oneidensis MR-1.

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Section: Role Of Riboflavins In Extracellular Electron Transfer In Picontrasting

confidence: 47%

Section: Role Of Riboflavins In Extracellular Electron Transfer In Pimentioning

confidence: 99%

The Role of Shewanella oneidensis MR‐1 Outer Surface Structures in Extracellular Electron Transfer

et al. 2010

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“…As this article went to press, von Canstein et al (45) reported secretion of flavins by multiple planktonic Shewanella cultures and noted a role for these compounds in azo dye decoloration and metal reduction. These results are consistent with our findings using biofilm cultures.…”

Section: Note Added In Proofmentioning

confidence: 99%

Shewanella secretes flavins that mediate extracellular electron transfer

Marsili¹,

Baron²,

Shikhare³

et al. 2008

Proc. Natl. Acad. Sci. U.S.A.

1,737

1,507

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Bacteria able to transfer electrons to metals are key agents in biogeochemical metal cycling, subsurface bioremediation, and corrosion processes. More recently, these bacteria have gained attention as the transfer of electrons from the cell surface to conductive materials can be used in multiple applications. In this work, we adapted electrochemical techniques to probe intact biofilms of Shewanella oneidensis MR-1 and Shewanella sp. MR-4 grown by using a poised electrode as an electron acceptor. This approach detected redox-active molecules within biofilms, which were involved in electron transfer to the electrode. A combination of methods identified a mixture of riboflavin and riboflavin-5 -phosphate in supernatants from biofilm reactors, with riboflavin representing the dominant component during sustained incubations (>72 h). Removal of riboflavin from biofilms reduced the rate of electron transfer to electrodes by >70%, consistent with a role as a soluble redox shuttle carrying electrons from the cell surface to external acceptors. Differential pulse voltammetry and cyclic voltammetry revealed a layer of flavins adsorbed to electrodes, even after soluble components were removed, especially in older biofilms. Riboflavin adsorbed quickly to other surfaces of geochemical interest, such as Fe(III) and Mn(IV) oxy(hydr)oxides. This in situ demonstration of flavin production, and sequestration at surfaces, requires the paradigm of soluble redox shuttles in geochemistry to be adjusted to include binding and modification of surfaces. Moreover, the known ability of isoalloxazine rings to act as metal chelators, along with their electron shuttling capacity, suggests that extracellular respiration of minerals by Shewanella is more complex than originally conceived.bioelectrochemistry ͉ biogeochemistry ͉ redox mediator ͉ riboflavin

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“…In addition, it has been proposed that secreted flavins, for example riboflavin (RF) and/or flavin mononucleotide (FMN), are reduced by MR-1 cells and then in their free form function as redox mediators for the Mtr pathway, thus facilitating EET reactions (Fig. 1A) (11,12). In support of this hypothesis, it was reported that the removal of flavin from the supernatants of systems with electrode-bound biofilms resulted in an ∼80% loss in microbial current production (12).…”

mentioning

confidence: 99%

Rate enhancement of bacterial extracellular electron transport involves bound flavin semiquinones

Okamoto

Hashimoto

Nealson

et al. 2013

Proc. Natl. Acad. Sci. U.S.A.

441

363

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Extracellular redox-active compounds, flavins and other quinones, have been hypothesized to play a major role in the delivery of electrons from cellular metabolic systems to extracellular insoluble substrates by a diffusion-based shuttling two-electron-transfer mechanism. Here we show that flavin molecules secreted by Shewanella oneidensis MR-1 enhance the ability of its outer-membrane c-type cytochromes (OM c-Cyts) to transport electrons as redox cofactors, but not free-form flavins. Whole-cell differential pulse voltammetry revealed that the redox potential of flavin was reversibly shifted more than 100 mV in a positive direction, in good agreement with increasing microbial current generation. Importantly, this flavin/OM c-Cyts interaction was found to facilitate a one-electron redox reaction via a semiquinone, resulting in a 10 3 -to 10 5 -fold faster reaction rate than that of free flavin. These results are not consistent with previously proposed redox-shuttling mechanisms but suggest that the flavin/OM c-Cyts interaction regulates the extent of extracellular electron transport coupled with intracellular metabolic activity.iron-reducing bacteria | electromicrobiology | microbial fuel cell | whole-cell voltammetry | flavin mononucleotide

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Secretion of Flavins by Shewanella Species and Their Role in Extracellular Electron Transfer

Abstract: Fe(III)-respiring bacteria such as

Cited by 790 publications

References 32 publications

The Role of Shewanella oneidensis MR‐1 Outer Surface Structures in Extracellular Electron Transfer

The Role of Shewanella oneidensis MR‐1 Outer Surface Structures in Extracellular Electron Transfer

Shewanella secretes flavins that mediate extracellular electron transfer

Rate enhancement of bacterial extracellular electron transport involves bound flavin semiquinones

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