Abstract
Proteins achieve efficient energy storage and conversion through electron transfer along a series of redox cofactors. Multiheme cytochromes are notable examples. These proteins transfer electrons over distance scales of several nanometers to >10 μm and in so doing they couple cellular metabolism with extracellular redox partners including electrodes. Here, we report pump-probe spectroscopy that provides a direct measure of the intrinsic rates of heme-heme electron transfer in this fascinating class of proteins. Our study took advantage of a spectrally unique His/Met-ligated heme introduced at a defined site within the decaheme extracellular MtrC protein of Shewanella oneidensis We observed rates of heme-to-heme electron transfer on the order of 109 s-1 (3.7 to 4.3 Å edge-to-edge distance), in good agreement with predictions based on density functional and molecular dynamics calculations. These rates are among the highest reported for ground-state electron transfer in biology. Yet, some fall 2 to 3 orders of magnitude below the Moser-Dutton ruler because electron transfer at these short distances is through space and therefore associated with a higher tunneling barrier than the through-protein tunneling scenario that is usual at longer distances. Moreover, we show that the His/Met-ligated heme creates an electron sink that stabilizes the charge separated state on the 100-μs time scale. This feature could be exploited in future designs of multiheme cytochromes as components of versatile photosynthetic biohybrid assemblies.
Highlights
Proteins achieve efficient energy storage and conversion through electron transfer along a series of redox cofactors
Notable examples are found in electromicrobiology where intracellular Electron transfer (ET) is coupled to transformation of extracellular redox partners
It is of interest to consider how the ET rates in multiheme cytochromes compare to those predicted by the Moser–Dutton ruler (M-DR) where the ΔG-optimized ET rates show an exponential decay with tunneling distance that is largely independent of the nature of the redox-active centers and the intervening protein structure [3, 4]
Summary
Proteins achieve efficient energy storage and conversion through electron transfer along a series of redox cofactors. These proteins transfer electrons over distance scales of several nanometers to >10 μm and in so doing they couple cellular metabolism with extracellular redox partners including electrodes. We observed rates of heme-to-heme electron transfer on the order of 109 s−1 (3.7 to 4.3 Å edge-to-edge distance), in good agreement with predictions based on density functional and molecular dynamics calculations. Biotechnologically relevant multiheme cytochromes including MtrC, MtrF, MtrA, and OmcS only computational estimates are available [21, 22] This situation represents a major gap in our empirical functional knowledge of these proteins; a molecular-scale understanding of the limiting factors for bacterial respiration and biotechnologies dependent on multiheme cytochromes is lacking. Deviations from exponential distance dependence are typically 1 to 2 orders of magnitude [3, 4, 23, 24] and could in some cases be explained in terms of the tunneling pathway model [25, 26]
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