Mechanisms of Manganese(II) Oxidation by Filamentous Ascomycete Fungi Vary With Species and Time as a Function of Secretome Composition

• Published in: Frontiers in microbiology Vol. 12; p. 610497
• Main Authors: Zeiner, Carolyn A, Purvine, Samuel O, Zink, Erika, Wu, Si, Paša-Tolić, Ljiljana, Chaput, Dominique L, Santelli, Cara M, Hansel, Colleen M
• Format: Journal Article
• Language: English
• Published: Switzerland Frontiers Media S.A 10.02.2021
• Subjects: biomineralization; filamentous fungi; geomicrobiology; manganese oxides; Microbiology; proteomics; secretome; filamentous fungi; geomicrobiology; biomineralization; proteomics; secretome; manganese oxides
• ISSN: 1664-302X; 1664-302X
• DOI: 10.3389/fmicb.2021.610497

Manganese (Mn) oxides are among the strongest oxidants and sorbents in the environment, and Mn(II) oxidation to Mn(III/IV) (hydr)oxides includes both abiotic and microbially-mediated processes. While white-rot Basidiomycete fungi oxidize Mn(II) using laccases and manganese peroxidases in association with lignocellulose degradation, the mechanisms by which filamentous Ascomycete fungi oxidize Mn(II) and a physiological role for Mn(II) oxidation in these organisms remain poorly understood. Here we use a combination of chemical and in-gel assays and bulk mass spectrometry to demonstrate secretome-based Mn(II) oxidation in three phylogenetically diverse Ascomycetes that is mechanistically distinct from hyphal-associated Mn(II) oxidation on solid substrates. We show that Mn(II) oxidative capacity of these fungi is dictated by species-specific secreted enzymes and varies with secretome age, and we reveal the presence of both Cu-based and FAD-based Mn(II) oxidation mechanisms in all 3 species, demonstrating mechanistic redundancy. Specifically, we identify candidate Mn(II)-oxidizing enzymes as tyrosinase and glyoxal oxidase in sp. SRC1lsM3a, bilirubin oxidase in sp. and AP3s5-JAC2a, and GMC oxidoreductase in all 3 species, including sp. DS3sAY3a. The diversity of the candidate Mn(II)-oxidizing enzymes identified in this study suggests that the ability of fungal secretomes to oxidize Mn(II) may be more widespread than previously thought.