Electron Transport in a Dioxygenase-Ferredoxin Complex: Long Range Charge Coupling between the Rieske and Non-Heme Iron Center

Wayne K Dawson; Ryota Jono; Tohru Terada; Kentaro Shimizu

doi:10.1371/journal.pone.0162031

Electron Transport in a Dioxygenase-Ferredoxin Complex: Long Range Charge Coupling between the Rieske and Non-Heme Iron Center

PLoS One. 2016 Sep 22;11(9):e0162031. doi: 10.1371/journal.pone.0162031. eCollection 2016.

Authors

Wayne K Dawson^{1

2

3}, Ryota Jono⁴, Tohru Terada^{1

5}, Kentaro Shimizu¹

Affiliations

¹ Department of Biotechnology, Graduate School of Agricultural and Life Sciences, The University of Tokyo, 1-1-1 Yayoi, Bunkyo-ku, Tokyo, 103-8657, Japan.
² Laboratory of Bioinformatics and Protein Engineering International Institute of Molecular and Cell Biology in Warsaw, ul Ks. Trojdena 4, 02-109, Warsaw, Poland.
³ Laboratory of Functional and Structural Genomics, Centre of New Technologies, University of Warsaw, Banacha 2C, 02-089, Warsaw, Poland.
⁴ Research Center for Advanced Science and Technology, The University of Tokyo Komaba, Meguro-ku, Tokyo, 153-8904, Japan.
⁵ Agricultural Bioinformatics Research Unit, Graduate School of Agricultural and Life Sciences, University of Tokyo, 1-1-1 Yayoi, Bunkyo-ku, Tokyo, 103-8657, Japan.

Abstract

Dioxygenase (dOx) utilizes stereospecific oxidation on aromatic molecules; consequently, dOx has potential applications in bioremediation and stereospecific oxidation synthesis. The reactive components of dOx comprise a Rieske structure Cys2[2Fe-2S]His2 and a non-heme reactive oxygen center (ROC). Between the Rieske structure and the ROC, a universally conserved Asp residue appears to bridge the two structures forming a Rieske-Asp-ROC triad, where the Asp is known to be essential for electron transfer processes. The Rieske and ROC share hydrogen bonds with Asp through their His ligands; suggesting an ideal network for electron transfer via the carboxyl side chain of Asp. Associated with the dOx is an itinerant charge carrying protein Ferredoxin (Fdx). Depending on the specific cognate, Fdx may also possess either the Rieske structure or a related structure known as 4-Cys-[2Fe-2S] (4-Cys). In this study, we extensively explore, at different levels of theory, the behavior of the individual components (Rieske and ROC) and their interaction together via the Asp using a variety of density function methods, basis sets, and a method known as Generalized Ionic Fragment Approach (GIFA) that permits setting up spin configurations manually. We also report results on the 4-Cys structure for comparison. The individual optimized structures are compared with observed spectroscopic data from the Rieske, 4-Cys and ROC structures (where information is available). The separate pieces are then combined together into a large Rieske-Asp-ROC (donor/bridge/acceptor) complex to estimate the overall coupling between individual components, based on changes to the partial charges. The results suggest that the partial charges are significantly altered when Asp bridges the Rieske and the ROC; hence, long range coupling through hydrogen bonding effects via the intercalated Asp bridge can drastically affect the partial charge distributions compared to the individual isolated structures. The results are consistent with a proton coupled electron transfer mechanism.

Grants and funding

This work was supported by the Platform for Drug Discovery, Informatics, and Structural Life Science from the Ministry of Education, Culture, Sports, Science and Technology, Japan. Additional support also came from the following: the European Commission (E.C.) [REGPOT grant FishMed, contract number 316125 to Jacek Kuźnicki in International Institute of Molecular and Cellular Biology in Warsaw] and from the Polish National Science Centre [grant numbers 2014/15/B/ST6/05082, 2013/09/B/NZ2/00121 to Dariusz Plewczynski in Centre of New Technologies].