Molecular basis of H2O2/O2.-/.OH discrimination during electrochemical activation of DyP peroxidases: The critical role of the distal residues

J Inorg Biochem. 2024 Dec 22:264:112816. doi: 10.1016/j.jinorgbio.2024.112816. Online ahead of print.

Abstract

Here, we show that the replacement of the distal residues Asp and/or Arg of the DyP peroxidases from Bacillus subtilis and Pseudomonas putida results in functional enzymes, albeit with spectroscopically perturbed active sites. All the enzymes can be activated either by the addition of exogenous H2O2 or by in situ electrochemical generation of the reactive oxygen species (ROS) OH, O2•- and H2O2. The latter method leads to broader and upshifted pH-activity profiles. Both WT enzymes exhibit a differential predominance of ROS involved in their electrochemical activation, which follows the order OH > O2•- > H2O2 for BsDyP and O2•- > H2O2 > OH for PpDyP. This ROS selectivity is preserved in mutants with unperturbed sites but is blurred out for distorted sites. The underlying molecular basis of the selectivity mechanisms is analysed through molecular dynamics simulations, which reveal distorted hydrogen bonding networks and higher throughput of the access tunnels in the variants exhibiting no selectivity. The electrochemical activation method provides superior performance for protein variants with a high prevalence of the alternative OH and O2•- species. These results constitute a promising advance towards engineering DyPs for electrocatalytic applications.

Keywords: Dye-decolorizing peroxidases; Oxoferryl intermediates; Reactive oxygen species; Resonance Raman spectroscopy; Site-directed mutagenesis; Spectroelectrochemistry.