Nanosecond heme-to-heme electron transfer rates in a multiheme cytochrome nanowire reported by a spectrally unique His/Met ligated heme

Van Wonderen, Jessica, Adamczyk, Katrin, Wu, Xiaojing, Jiang, Xiuyun, Piper, Samuel, Hall, Christopher, Edwards, Marcus, Clarke, Tom, Zhang, Huijie, Jeuken, Lars, Sazanovich, Igor, Towrie, Michael, Blumberger, Jochen, Meech, Steve ORCID: https://orcid.org/0000-0001-5561-2782 and Butt, Julea ORCID: https://orcid.org/0000-0002-9624-5226 (2021) Nanosecond heme-to-heme electron transfer rates in a multiheme cytochrome nanowire reported by a spectrally unique His/Met ligated heme. Proceedings of the National Academy of Sciences, 118 (39). ISSN 0027-8424

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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 (3.7-4.3 Å edge-to-edge distance), in good agreement with predictions based on density functional and molecular dynamics calculations. These rates are amongst the highest reported for ground state electron transfer in biology. Yet, some fall 2-3 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 microsecond time scale. This feature could be exploited in future designs of multiheme cytochromes as components of versatile photosynthetic biohybrid assemblies.

Item Type: Article
Additional Information: ACKNOWLEDGMENTS. We are grateful to the Science and Technology Facilities Council for access to the ULTRA laser facility (Application 18130011) and the Engineering and Physical Sciences Research Council UK National Mass Spectrometry Facility at Swansea University for characterization of [Ru(4-bromomethyl-4’-methylbipyridine)(2,2’-bipyridine)2](PF6)2. We are grateful to Diamond Light Source for beamtime (proposal mx25108) and the staff of beamline I04 for assistance with crystal testing and data collection, to Dr. Simone Payne for assistance with protein preparation, and to Anna Ondrácková for preliminary redox characterization of Ru-MtrC proteins. Funding was from the UK Engineering and Physical Sciences Research Council (EP/M001989/1, EP/M001946/1, EP/N033647/1), UK Biotechnology and Biological Sciences Research Council (BB/S002499/1, BB/S000704/1, BB/P01819X/1, and a Doctoral Training Partnership PhD studentship to S.E.H.P.) and the European Research
Uncontrolled Keywords: electron transfer,moser–dutton ruler,pump-probe spectroscopy,ru(ii)tris(bipyridine),shewanella,4* ,/dk/atira/pure/researchoutput/REFrank/4_
Faculty \ School: Faculty of Science > School of Chemistry
Faculty of Science > School of Biological Sciences
Faculty of Science > School of Natural Sciences
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Depositing User: LivePure Connector
Date Deposited: 10 Aug 2021 01:28
Last Modified: 30 Oct 2022 00:53
URI: https://ueaeprints.uea.ac.uk/id/eprint/81027
DOI: 10.1073/pnas.2107939118

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