Abstract
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 Stagonospora sp. SRC1lsM3a, bilirubin oxidase in Stagonospora sp. and Paraconiothyrium sporulosum AP3s5-JAC2a, and GMC oxidoreductase in all 3 species, including Pyrenochaeta 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.
Highlights
Manganese (Mn) (III/IV)oxide minerals are ubiquitous in the environment, including terrestrial and aquatic systems
While the Pyrenochaeta sp. secretome did not oxidize Mn(II) after 7 days (Figure 1B), it exhibited a peak Mn(IV) production rate [708 μM Mn(IV) produced μg protein−1 hr−1] at 14 days, the highest we observed among the 3 species, and this rate significantly dropped off by 21 days (P = 3.9 × 10−6)
For all 3 fungi, < 10 kDa filtrate remaining after secretome harvest did not exhibit Mn(II) oxidative capacity measurable with Leucoberbelin blue (LBB)
Summary
Manganese (Mn) (III/IV) (hydr)oxide minerals are ubiquitous in the environment, including terrestrial and aquatic systems. Due to their small particle size, large surface area, and high sorptive and oxidative capacities, Mn oxides are among the most reactive mineral phases in the environment. The mechanisms of Mn(II) oxidation to Mn(III/IV) (hydr)oxides include both abiotic and microbially-mediated processes. Complexation of Mn(II) to destabilizing ligands, mineral surfaces, and/or enzyme active sites removes this energetic barrier, allowing for rapid O2-induced Mn(II) oxidation to Mn(III), which may be further oxidized or disproportionate to Mn(II) and Mn(IV) to precipitate Mn oxides (Bargar et al, 2005; Duckworth and Sposito, 2005; Madden and Hochella, 2005; Learman et al, 2011b). A large and diverse group of Mn(II)-oxidizing bacteria (Tebo et al, 2004), fungi (Miyata et al, 2007), and algae (Chaput et al, 2019) have been identified to date, and research on the underlying mechanisms has begun to elucidate the roles of key enzymes and reactive metabolites
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