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

Research output: Contribution to journalArticlepeer-review

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.

Original languageEnglish (US)
Article number610497
JournalFrontiers in Microbiology
Volume12
DOIs
StatePublished - Feb 10 2021

Bibliographical note

Funding Information:
The authors thank Joshua Aldrich (EMSL) and Michele Clamp (Harvard) for bioinformatic analyses at various stages of this project, and Therese R. Clauss (EMSL) for expertise in LC/MS/MS instrumentation throughout this project. The authors disclaim endorsement of any products mentioned in this manuscript. Funding. This work was supported by the National Science Foundation, grant numbers EAR-1249489 and CBET-1336496, both awarded to CH, by a JGI-EMSL Collaborative Science Initiative grant (proposal number 48100) awarded to CH and CS, and by the University of St. Thomas. Personal support for CZ was also provided by Harvard University and by a Ford Foundation Predoctoral Fellowship administered by the National Academies. A portion of this research was performed under the Facilities Integrating Collaborations for User Science (FICUS) program and used resources at the DOE Joint Genome Institute and the Environmental Molecular Sciences Laboratory (grid.436923.9), which are DOE Office of Science User Facilities. Both facilities are sponsored by the Biological and Environmental Research Program and operated under Contract Nos. DE-AC02-05CH11231 (JGI) and DE-AC05-76RL01830 (EMSL). Part of this research was performed at the Bauer Core Facility of the FAS Center for Systems Biology at Harvard University. A portion of the bioinformatics analysis was performed at Harvard?s FAS Research Computing facility.

Publisher Copyright:
© Copyright © 2021 Zeiner, Purvine, Zink, Wu, Paša-Tolić, Chaput, Santelli and Hansel.

Keywords

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

PubMed: MeSH publication types

  • Journal Article

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