Abstract
The bacterium Shewanella oneidensis has evolved a sophisticated electron transfer (ET) machinery to export electrons from the cytosol to extracellular space during extracellular respiration. At the heart of this process are decaheme proteins of the Mtr pathway, MtrC and MtrF, located at the external face of the outer bacterial membrane. Crystal structures have revealed that these proteins bind 10 c-type hemes arranged in the peculiar shape of a staggered cross that trifurcates the electron flow, presumably to reduce extracellular substrates while directing electrons to neighboring multiheme cytochromes at either side along the membrane. Especially intriguing is the design of the heme junctions trifurcating the electron flow: they are made of coplanar and T-shaped heme pair motifs with relatively large and seemingly unfavorable tunneling distances. Here, we use electronic structure calculations and molecular simulations to show that the side chains of the heme rings, in particular the cysteine linkages inserting in the space between coplanar and T-shaped heme pairs, strongly enhance electronic coupling in these two motifs. This results in an [Formula: see text]-fold speedup of ET steps at heme junctions that would otherwise be rate limiting. The predicted maximum electron flux through the solvated proteins is remarkably similar for all possible flow directions, suggesting that MtrC and MtrF shuttle electrons with similar efficiency and reversibly in directions parallel and orthogonal to the outer membrane. No major differences in the ET properties of MtrC and MtrF are found, implying that the different expression levels of the two proteins during extracellular respiration are not related to redox function.
Highlights
The coupling calculations were carried out for two quantum mechanical (QM) models on structures extracted from the molecular dynamics (MD) run: one where the two bis-His hemes are modeled by unsubstituted Fe-porphin rings axially ligated by two N-methyl imidazoles, hereafter referred to as the minimum model, and one where, in addition, all of the side chains of both heme rings are included, hereafter referred to as the large model
Details on the MD simulations and the density functional theory (DFT)-based coupling calculations can be found in Materials and Methods and SI Appendix
The thermally averaged couplings for each heme pair of MtrC are depicted in Fig. 2B, clearly illustrating how the couplings decrease from relatively large values for the stacked motif at electron input and exit sites of the octaheme chain to smaller values for the T-shaped and coplanar motifs in the middle of the protein
Summary
Adjacent MtrCAB complexes are thought to interact via the tetraheme chains of MtrC to facilitate micrometer-long electron transfer along the outer membrane as observed by conductive atomic force microscopy (c-AFM) [22], while the octaheme chains support ET away from the membrane and onto extracellular substrates. In this way, the heme cross motif helps supply the surface of the membrane with electrons while reducing extracellular substrates. Does this protein transfer electrons well in the direction parallel to the membrane and away from it?
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