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A Dynamic Water Channel Affects O<sub>2</sub> Stability in [FeFe]‐Hydrogenases

Claudia Brocks, Chandan K. Das, Jifu Duan, Shanika Yadav, Ulf‐Peter Apfel, Subhasri Ghosh, Eckhard Hofmann, Martin Winkler, Vera Engelbrecht, Lars V. Schäfer, Thomas Happe

2023ChemSusChem13 citationsDOIOpen Access PDF

Abstract

Abstract [FeFe]‐hydrogenases are capable of reducing protons at a high rate. However, molecular oxygen (O 2 ) induces the degradation of their catalytic cofactor, the H‐cluster, which consists of a cubane [4Fe4S] subcluster (4Fe H ) and a unique diiron moiety (2Fe H ). Previous attempts to prevent O 2 ‐induced damage have focused on enhancing the protein's sieving effect for O 2 by blocking the hydrophobic gas channels that connect the protein surface and the 2Fe H . In this study, we aimed to block an O 2 diffusion pathway and shield 4Fe H instead. Molecular dynamics (MD) simulations identified a novel water channel (W H ) surrounding the H‐cluster. As this hydrophilic path may be accessible for O 2 molecules we applied site‐directed mutagenesis targeting amino acids along W H in proximity to 4Fe H to block O 2 diffusion. Protein film electrochemistry experiments demonstrate increased O 2 stabilities for variants G302S and S357T, and MD simulations based on high‐resolution crystal structures confirmed an enhanced local sieving effect for O 2 in the environment of the 4Fe H in both cases. The results strongly suggest that, in wild type proteins, O 2 diffuses from the 4Fe H to the 2Fe H . These results reveal new strategies for improving the O 2 stability of [FeFe]‐hydrogenases by focusing on the O 2 diffusion network near the active site.

Topics & Concepts

HydrogenaseChemistryWater splittingMaterials scienceChemical engineeringNanotechnologyHydrogenCatalysisPhotocatalysisEngineeringBiochemistryOrganic chemistryMetalloenzymes and iron-sulfur proteinsElectrocatalysts for Energy ConversionMetal-Catalyzed Oxygenation Mechanisms