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Fluctuating hydrogen-bond networks govern anomalous electron transfer kinetics in a blue copper protein

Kretchmer, Joshua S. and Boekelheide, Nicholas and Warren, Jeffrey J. and Winkler, Jay R. and Gray, Harry B. and Miller, Thomas F., III (2018) Fluctuating hydrogen-bond networks govern anomalous electron transfer kinetics in a blue copper protein. Proceedings of the National Academy of Sciences of the United States of America, 115 (24). pp. 6129-6134. ISSN 0027-8424. PMCID PMC6004490. http://resolver.caltech.edu/CaltechAUTHORS:20180529-142106727

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Abstract

We combine experimental and computational methods to address the anomalous kinetics of long-range electron transfer (ET) in mutants of Pseudomonas aeruginosa azurin. ET rates and driving forces for wild type (WT) and three N47X mutants (X = L, S, and D) of Ru(2,2′-bipyridine)2 (imidazole)(His83) azurin are reported. An enhanced ET rate for the N47L mutant suggests either an increase of the donor–acceptor (DA) electronic coupling or a decrease in the reorganization energy for the reaction. The underlying atomistic features are investigated using a recently developed nonadiabatic molecular dynamics method to simulate ET in each of the azurin mutants, revealing unexpected aspects of DA electronic coupling. In particular, WT azurin and all studied mutants exhibit more DA compression during ET (>2 Å) than previously recognized. Moreover, it is found that DA compression involves an extended network of hydrogen bonds, the fluctuations of which gate the ET reaction, such that DA compression is facilitated by transiently rupturing hydrogen bonds. It is found that the N47L mutant intrinsically disrupts this hydrogen-bond network, enabling particularly facile DA compression. This work, which reveals the surprisingly fluctional nature of ET in azurin, suggests that hydrogen-bond networks can modulate the efficiency of long-range biological ET.


Item Type:Article
Related URLs:
URLURL TypeDescription
https://doi.org/10.1073/pnas.1805719115DOIArticle
https://www.pnas.org/lookup/suppl/doi:10.1073/pnas.1805719115/-/DCSupplementalPublisherSupporting Information
https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6004490PubMed CentralArticle
ORCID:
AuthorORCID
Kretchmer, Joshua S.0000-0003-3468-0481
Winkler, Jay R.0000-0002-4453-9716
Miller, Thomas F., III0000-0002-1882-5380
Additional Information:© 2018 the Author(s). Published by PNAS. This open access article is distributed under Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND). Edited by Michael L. Klein, Temple University, Philadelphia, PA, and approved May 4, 2018 (received for review April 3, 2018). Published ahead of print May 29, 2018. This work was supported by the NIH under Award R01DK019038 (to H.B.G. and J.R.W.) and by the NSF under Award CHE-1611581 (to T.F.M.). Additional support was provided by NIH Grant GM095037 (to J.J.W.), the Arnold and Mabel Beckman Foundation, and NSF Grant DGE-1144469 (to J.S.K.). Author contributions: J.S.K., N.B., J.J.W., J.R.W., H.B.G., and T.F.M. designed research; J.S.K., N.B., and J.J.W. performed research; J.S.K., N.B., J.J.W., J.R.W., H.B.G., and T.F.M. analyzed data; and J.S.K., N.B., J.J.W., J.R.W., H.B.G., and T.F.M. wrote the paper. The authors declare no conflict of interest. This article is a PNAS Direct Submission. This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1805719115/-/DCSupplemental.
Funders:
Funding AgencyGrant Number
NIHR01DK019038
NSFCHE-1611581
NIHGM095037
Arnold and Mabel Beckman FoundationUNSPECIFIED
NSF Graduate Research FellowshipDGE-1144469
Subject Keywords:electron transfer; azurin; ring polymer molecular dynamics; Marcus theory; protein dynamics
PubMed Central ID:PMC6004490
Record Number:CaltechAUTHORS:20180529-142106727
Persistent URL:http://resolver.caltech.edu/CaltechAUTHORS:20180529-142106727
Official Citation:Fluctuating hydrogen-bond networks govern anomalous electron transfer kinetics in a blue copper protein. Joshua S. Kretchmer, Nicholas Boekelheide, Jeffrey J. Warren, Jay R. Winkler, Harry B. Gray, Thomas F. Miller. Proceedings of the National Academy of Sciences Jun 2018, 115 (24) 6129-6134; DOI: 10.1073/pnas.1805719115
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:86677
Collection:CaltechAUTHORS
Deposited By: Tony Diaz
Deposited On:29 May 2018 21:35
Last Modified:20 Jun 2018 16:16

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