Department/School

Biology

Date

2021

Document Type

Article

Keywords

manganese oxides, filamentous fungi, geomicrobiology, proteomics, biomineralization, secretome

DOI

https://doi.org/10.3389/fmicb.2021.610497

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.

Published in

Frontiers in Microbiology

Citation/Other Information

Zeiner CA, Purvine SO, Zink E, Wu S, Paša-Tolić L, Chaput DL, Santelli CM, Hansel CM. 2021. Mechanisms of manganese(II) oxidation by filamentous Ascomycete fungi vary with species and time as a function of secretome composition. Frontiers in Microbiology 12: 610497. DOI: 10.3389/fmicb.2021.610497.

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