Redox-linked conformation change and electron transfer between monoheme c-type cytochromes and oxides (original) (raw)
Related papers
Cytochrome c interaction with hematite (alpha-Fe2O3) surfaces
The interaction of metalloproteins such as cytochromes with oxides is of interest for a number of reasons, including molecular catalysis of environmentally important mineral-solution electron transfer reactions (e.g., dehalogenations) and photovoltaic applications. Iron reduction by bacteria, thought to be cytochrome mediated, is of interest for geochemical and environmental remediation reasons. As a baseline for understanding cytochrome interaction with ferric oxide surfaces, we report on the interaction of mitochondrial cytochrome c (Mcc), a well-studied protein, with hematite (-Fe2O3) surfaces. Mcc sorbs strongly to hematite from aqueous solution in a narrow pH range corresponding to opposite charge on Mcc and hematite (between pH 8.5 and 10, Mcc is positively charged and hematite surfaces are negatively charged). Cyclic voltammetry of Mcc using hematite electrodes gives redox potentials characteristic of Mcc in a native conformational state, with no evidence for unfolding on the hematite surface. Atomic force microscopy imaging is consistent with a loosely attached adsorbate that is easily deformed by the AFM tip. In phosphate-containing solution, Mcc adhers to the surface more strongly. These results establish hematite as a viable material for electrochemical and spectroscopic characterization of cytochrome–mineral interaction.
Sorption and direct electrochemistry of mitochondrial cytochrome c on hematite surfaces
The interaction of cytochromes (heme proteins) with mineral surfaces is important from an environmental perspective (e.g. heavy metal remediation and reductive dehalogenation reactions), for designing biosensors and bioanalytical systems, and for emerging photovoltaic applications. In addition, the cytochrome studied here shares properties with some cytochromes from Fe-reducing bacteria and its general behavior sheds light on how other cytochromes might behave during Fe(III) reduction. The objectives of this study were to characterize the direct electrochemistry and sorption mechanism of horse heart ferricytochrome c (a mitochondrial cytochrome referred to as Hcc) on hematite surfaces as a function of pH, time of sorption and ionic strength. Hcc sorption on hematite mainly occurs between pH 8 and 10, the pH range in which hematite surfaces and Hcc are oppositely charged. Calculated net attractive forces correspond closely with the pH range of peak sorption, suggesting that sorption is mainly electrostatically controlled. Hcc sorption with ionic strength is consistent with this conclusion. The pH-dependent conformation of Hcc sorbed on hematite appears to be different from that in solution as indicated by UV- visible spectroscopy and its more negative reduction potential compared to native Hcc. Sorption kinetics were rapid and pH-independent across the pH range 3ÿ10 with slow conformational changes occurring at >60 h. Our results suggest that the electrostatic attraction of the cytochrome towards the surface orient the cytochrome for favorable electron transfer between the heme group of the cytochrome and hematite.
Kinetic studies on the electron transfer between bacterial c-type cytochromes and metal oxides
Journal of Electroanalytical Chemistry, 1998
Cyclic voltammetry was used to investigate the kinetics of the electron transfer between various soluble or solid metal oxides, and polyheme c-type cytochromes from Desulfuromonas acetoxidans and Desulfo6ibrio. The second order rate constant for the catalytic reduction of soluble chromate ions by Desulfuromonas acetoxidans cytochrome c 7 was found to be 6 × 10 5 M − 1 s − 1 . By using the membrane electrode technology, it has been shown that the catalytic process for Cr(VI) reduction is efficient even when the cytochrome is entrapped in the close vicinity of the electrode surface. Moreover, this proceeding allowed the catalytic reduction of solid metal oxides such as manganese(IV), vanadium(V) and iron(III) oxides to be performed. Results suggest that the metal reductase activity of a microorganism is governed by its c-type cytochrome content. Furthermore, only cytochromes with bishistidinyl heme iron coordination act as metal reducers whereas mitochondrial c-type cytochromes do not. This approach opens new pathways for the use of sulfur or sulfate bacteria in the bioremediation of metal contaminated waters and waste streams. Processes involving the use of entrapped enzymes reactors could be developed according to the metal reducing activity of their polyheme c-type cytochromes.
Biochemistry. Biokhimii͡a, 2014
Bacteria utilizing insoluble mineral forms of metal oxides as electron acceptors in respiratory processes are widespread in the nature. The electron transfer from a pool of reduced quinones in the cytoplasmic membrane across the periplasm to the bacterial outer membrane and then to an extracellular acceptor is a key step in bacterial dissimilatory metal reduction. Multiheme cytochromes c play a crucial role in the extracellular electron transfer. The bacterium Shewanella oneidensis MR-1 was used as a model organism to study the mechanism of extracellular electron transport. In this review, we discuss recent data on the composition, structures, and functions of multiheme cytochromes c and their functional complexes responsible for extracellular electron transport in Shewanella oneidensis.
The Journal of biological chemistry, 2018
Many subsurface microorganisms couple their metabolism to the reduction or oxidation of extracellular substrates. For example, anaerobic mineral-respiring bacteria can use external metal oxides as terminal electron acceptors during respiration. Porin-cytochrome complexes facilitate the movement of electrons generated through intracellular catabolic processes across the bacterial outer membrane to these terminal electron acceptors. In the mineral-reducing model bacterium Shewanella oneidensis MR-1, this complex is composed of two decaheme cytochromes (MtrA and MtrC) and an outer-membrane β-barrel (MtrB). However, the structures and mechanisms by which porin-cytochrome complexes transfers electrons are unknown. Here, we used small-angle neutron scattering (SANS) to study the molecular structure of the transmembrane complexes MtrAB and MtrCAB. Ab initio modeling of the scattering data yielded a molecular envelope with dimensions of ~105 × 60 × 35 Å for MtrAB and ~170 × 60 × 45 Å for Mt...
Journal of Bacteriology, 2007
Shewanella oneidensis MR-1 is purported to express outer membrane cytochromes (e.g., MtrC and OmcA) that transfer electrons directly to Fe(III) in a mineral during anaerobic respiration. A prerequisite for this type of reaction would be the formation of a stable bond between a cytochrome and an iron oxide surface. Atomic force microscopy (AFM) was used to detect whether a specific bond forms between a hematite (Fe 2 O 3 ) thin film, created with oxygen plasma-assisted molecular beam epitaxy, and recombinant MtrC or OmcA molecules coupled to gold substrates. Force spectra displayed a unique force signature indicative of a specific bond between each cytochrome and the hematite surface. The strength of the OmcA-hematite bond was approximately twice that of the MtrC-hematite bond, but direct binding to hematite was twice as favorable for MtrC. Reversible folding/unfolding reactions were observed for mechanically denatured MtrC molecules bound to hematite. The force measurements for the hematite-cytochrome pairs were compared to spectra collected for an iron oxide and S. oneidensis under anaerobic conditions. There is a strong correlation between the whole-cell and pure-protein force spectra, suggesting that the unique binding attributes of each cytochrome complement one another and allow both MtrC and OmcA to play a prominent role in the transfer of electrons to Fe(III) in minerals. Finally, by comparing the magnitudes of binding force for the whole-cell versus pure-protein data, we were able to estimate that a single bacterium of S. oneidensis (2 by 0.5 m) expresses ϳ10 4 cytochromes on its outer surface.