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

Carolyn A Zeiner; Samuel O Purvine; Erika Zink; Si Wu; Ljiljana Paša-Tolić; Dominique L Chaput; Cara M Santelli; Colleen M Hansel

doi:10.3389/fmicb.2021.610497

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

Front Microbiol. 2021 Feb 10:12:610497. doi: 10.3389/fmicb.2021.610497. eCollection 2021.

Authors

Carolyn A Zeiner¹, Samuel O Purvine², Erika Zink³, Si Wu⁴, Ljiljana Paša-Tolić², Dominique L Chaput⁵, Cara M Santelli⁶, Colleen M Hansel⁷

Affiliations

¹ Department of Biology, University of St. Thomas, Saint Paul, MN, United States.
² Environmental Molecular Sciences Laboratory, Pacific Northwest National Laboratory, Richland, WA, United States.
³ Biological Sciences Laboratory, Pacific Northwest National Laboratory, Richland, WA, United States.
⁴ Department of Chemistry and Biochemistry, The University of Oklahoma, Norman, OK, United States.
⁵ Biosciences, Geoffrey Pope Building, University of Exeter, Exeter, United Kingdom.
⁶ Department of Earth and Environmental Sciences, University of Minnesota, Minneapolis, MN, United States.
⁷ Department of Marine Chemistry & Geochemistry, Woods Hole Oceanographic Institution, Woods Hole, MA, United States.

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.

Keywords: biomineralization; filamentous fungi; geomicrobiology; manganese oxides; proteomics; secretome.