Electronic structural flexibility of heterobimetallic Mn/Fe cofactors: R2lox and R2c proteins

Hannah S. Shafaat, Julia J. Griese, Dimitrios A. Pantazis, Katarina Roos, Charlotta S. Andersson, Ana Popović-Bijelić, Astrid Gräslund, Per E.M. Siegbahn, Frank Neese, Wolfgang Lubitz, Martin Högbom, Nicholas Cox*

*Corresponding author for this work

Research output: Contribution to journalArticlepeer-review

32 Citations (Scopus)

Abstract

The electronic structure of the Mn/Fe cofactor identified in a new class of oxidases (R2lox) described by Andersson and Hö gbom [Proc. Natl. Acad. Sci. U.S.A. 2009, 106, 5633] is reported. The R2lox protein is homologous to the small subunit of class Ic ribonucleotide reductase (R2c) but has a completely different in vivo function. Using multifrequency EPR and related pulse techniques, it is shown that the cofactor of R2lox represents an antiferromagnetically coupled MnIII/ FeIII dimer linked by a μ-hydroxo/bis-μ-carboxylato bridging network. The MnIII ion is coordinated by a single water ligand. The R2lox cofactor is photoactive, converting into a second form ( R2lox Photo) upon visible illumination at cryogenic temperatures (77 K) that completely decays upon warming. This second, unstable form of the cofactor more closely resembles the MnIII/FeIII cofactor seen in R2c. It is shown that the two forms of the R2lox cofactor differ primarily in terms of the local site geometry and electronic state of the MnIII ion, as best evidenced by a reorientation of its unique 55Mn hyperfine axis. Analysis of the metal hyperfine tensors in combination with density functional theory (DFT) calculations suggests that this change is triggered by deprotonation of the μ-hydroxo bridge. These results have important consequences for the mixed-metal R2c cofactor and the divergent chemistry R2lox and R2c perform.

Original languageEnglish
Pages (from-to)13399-13409
Number of pages11
JournalJournal of the American Chemical Society
Volume136
Issue number38
DOIs
Publication statusPublished - 24 Sept 2014
Externally publishedYes

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