Mechanism of Reduction of Aqueous U(V)-dpaea and Solid-Phase U(VI)-dpaea Complexes: The Role of Multiheme c‑Type Cytochromes

• Published in: Environmental science & technology Vol. 57; no. 19; pp. 7537 - 7546
• Main Authors: Molinas, Margaux, Meibom, Karin Lederballe, Faizova, Radmila, Mazzanti, Marinella, Bernier-Latmani, Rizlan
• Format: Journal Article
• Language: English
• Published: United States American Chemical Society 16-05-2023
• Subjects: Aqueous solutions; Cytochrome; Cytochromes; Deletion mutant; Electron transfer; Electron Transport; Electrons; Major histocompatibility complex; Membranes; Occurrence, Fate, and Transport of Aquatic and Terrestrial Contaminants; Oxidation-Reduction; Reduction; Shewanella - chemistry; Solid phases; bioremediation; extracellular electron transfer; reduction mechanism; pentavalent U; solid phase U(VI)
• ISSN: 0013-936X; 1520-5851
• DOI: 10.1021/acs.est.3c00666

The biological reduction of soluble U­(VI) complexes to form immobile U­(IV) species has been proposed to remediate contaminated sites. It is well established that multiheme c-type cytochromes (MHCs) are key mediators of electron transfer to aqueous phase U­(VI) complexes for bacteria such as Shewanella oneidensis MR-1. Recent studies have confirmed that the reduction proceeds via a first electron transfer forming pentavalent U­(V) species that readily disproportionate. However, in the presence of the stabilizing aminocarboxylate ligand, dpaea2– (dpaeaH2bis­(pyridyl-6-methyl-2-carboxylate)-ethylamine), biologically produced U­(V) persisted in aqueous solution at pH 7. We aim to pinpoint the role of MHC in the reduction of U­(V)-dpaea and to establish the mechanism of solid-phase U­(VI)-dpaea reduction. To that end, we investigated U-dpaea reduction by two deletion mutants of S. oneidensis MR-1–one lacking outer membrane MHCs and the other lacking all outer membrane MHCs and a transmembrane MHC–and by the purified outer membrane MHC, MtrC. Our results suggest that solid-phase U­(VI)-dpaea is reduced primarily by outer membrane MHCs. Additionally, MtrC can directly transfer electrons to U­(V)-dpaea to form U­(IV) species but is not strictly necessary, underscoring the primary involvement of outer membrane MHCs in the reduction of this pentavalent U species but not excluding that of periplasmic MHCs.