Purification and Magneto-optical Spectroscopic Characterization of Cytoplasmic Membrane and Outer Membrane Multiheme c-Type Cytochromes from Shewanella frigidimarina NCIMB400

Field, Sarah J.; Dobbin, Paul S.; Cheesman, Myles R.; Watmough, Nicholas J.; Thomson, Andrew J.; Richardson, David J.

doi:10.1074/jbc.275.12.8515

Cited by 107 publications

(119 citation statements)

References 39 publications

Supporting

Mentioning

109

Contrasting

Order By: Relevance

“…Oxidation of lactate to acetate (E°Ј ϭ Ϫ0.42 V) linked to riboflavin reduction (E°Ј ϭ Ϫ0.21 V) provides Ϫ81 kJ/mol free energy, which, at a cost of ATP synthesis of Ϸ60 kJ/mol ATP, allows 1.5 ATP/lactate. This estimate is similar to those based on midpoint potentials of outer membrane cytochromes implicated in metal reduction by Shewanella such as OmcA (Ϫ0.24 to Ϫ0.32 V) (21), and MtrC (approximately Ϫ0.1 V) (22), making 1.5 ATP/ lactate a conservative assumption for ATP yield.…”

Section: Resultssupporting

confidence: 60%

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

View full text Add to dashboard Cite

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

show abstract

Section: Resultssupporting

confidence: 60%

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

View full text Add to dashboard Cite

show abstract

“…This configuration has been shown from modeling to be optimal for electron transfer to insoluble minerals (14) and so this heme is well placed to interact with minerals in the extracellular environment. Consistent with this, electron exchange with solid graphite electrodes probed by PFV is fast, a feature in common with OmcA and MtrC (29,30,32). It is then perhaps surprising that oxidation of reduced MtrF by suspensions of solid ferrihydrite is very slow.…”

Section: Discussionsupporting

confidence: 50%

Structure of a bacterial cell surface decaheme electron conduit

Clarke

Edwards

Gates

et al. 2011

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

Self Cite

308

375

View full text Add to dashboard Cite

Some bacterial species are able to utilize extracellular mineral forms of iron and manganese as respiratory electron acceptors. In Shewanella oneidensis this involves decaheme cytochromes that are located on the bacterial cell surface at the termini of transouter-membrane electron transfer conduits. The cell surface cytochromes can potentially play multiple roles in mediating electron transfer directly to insoluble electron sinks, catalyzing electron exchange with flavin electron shuttles or participating in extracellular intercytochrome electron exchange along "nanowire" appendages. We present a 3.2-Å crystal structure of one of these decaheme cytochromes, MtrF, that allows the spatial organization of the 10 hemes to be visualized for the first time. The hemes are organized across four domains in a unique crossed conformation, in which a staggered 65-Å octaheme chain transects the length of the protein and is bisected by a planar 45-Å tetraheme chain that connects two extended Greek key split β-barrel domains. The structure provides molecular insight into how reduction of insoluble substrate (e.g., minerals), soluble substrates (e.g., flavins), and cytochrome redox partners might be possible in tandem at different termini of a trifurcated electron transport chain on the cell surface.c-type cytochromes | iron respiration | MtrC | multiheme

show abstract

“…These proteins include CymA, a tetraheme c-type cytochrome anchored to the inner membrane that serves as a MQH 2 dehydrogenase [8,12,20,43,44]; Stc, a 12-kDa tetraheme periplasmic c-type cytochrome [15,45] and the periplasmic decaheme cytochrome MtrA [10] (Fig. 1).…”

Section: Discussionmentioning

confidence: 99%

“…Electron transport proteins proposed to be involved in Fe(III) respiration in Shewanella oneidensis MR-1 include an inner-membrane periplasmic tetraheme quinol dehydrogenase (CymA) [8,12], two periplasmic decaheme cytochromes (MtrD and MtrA) [10,13], periplasmic tetraheme cytochrome (Stc) [14,15], the cytochrome domain of Fe(III)-induced flavocytochrome c 3 , [16] two putative outer-membrane b-barrel proteins (MtrE and MtrB) [17][18][19] and three outer-membrane decaheme cytochromes (MtrF, OmcA and MtrC) [11,18,20,21]. Although genetic studies have identified specific proteins that are involved in Fe(III) respiration in Shewanella sp.…”

Section: Introductionmentioning

confidence: 99%

Characterization of Shewanella oneidensis MtrC: a cell-surface decaheme cytochrome involved in respiratory electron transport to extracellular electron acceptors

et al. 2007

Self Cite

View full text Add to dashboard Cite

MtrC is a decaheme c-type cytochrome associated with the outer cell membrane of Fe(III)-respiring species of the Shewanella genus. It is proposed to play a role in anaerobic respiration by mediating electron transfer to extracellular mineral oxides that can serve as terminal electron acceptors. The present work presents the first spectropotentiometric and voltammetric characterization of MtrC, using protein purified from Shewanella oneidensis MR-1. Potentiometric titrations, monitored by UV-vis absorption and electron paramagnetic resonance (EPR) spectroscopy, reveal that the hemes within MtrC titrate over a broad potential range spanning between approximately +100 and approximately À500 mV (vs. the standard hydrogen electrode). Across this potential window the UVvis absorption spectra are characteristic of low-spin c-type hemes and the EPR spectra reveal broad, complex features that suggest the presence of magnetically spin-coupled lowspin c-hemes. Non-catalytic protein film voltammetry of MtrC demonstrates reversible electrochemistry over a potential window similar to that disclosed spectroscopically. The voltammetry also allows definition of kinetic properties of MtrC in direct electron exchange with a solid electrode surface and during reduction of a model Fe(III) substrate. Taken together, the data provide quantitative information on the potential domain in which MtrC can operate.

show abstract

Purification and Magneto-optical Spectroscopic Characterization of Cytoplasmic Membrane and Outer Membrane Multiheme c-Type Cytochromes from Shewanella frigidimarina NCIMB400

Cited by 107 publications

References 39 publications

Shewanella secretes flavins that mediate extracellular electron transfer

Shewanella secretes flavins that mediate extracellular electron transfer

Structure of a bacterial cell surface decaheme electron conduit

Characterization of Shewanella oneidensis MtrC: a cell-surface decaheme cytochrome involved in respiratory electron transport to extracellular electron acceptors

Contact Info

Product

Resources

About