Mechanisms of manganese(II) oxidation by filamentous ascomycete fungi vary with species and time as a function of secretome composition

© The Author(s), 2021. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Zeiner, C. A., Purvine, S. O., Zink, E., Wu, S., Pasa-Tolic, L., Chaput, D. L., Santelli, C. M., & Hansel, C. M. Mechanisms of manganese(II) oxidation by filamentous ascomycete fungi vary with species and time as a function of secretome composition. Frontiers in Microbiology, 12, (2021): 610497, https://doi.org/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 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.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

Functional diversification of maize RNA polymerase IV and V subtypes via alternative catalytic subunits.

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EMSL Geochemistry, Biogeochemistry and Subsurface Science-Science Theme Advisory Panel Meeting

This report covers the topics of discussion and the recommendations of the panel members. On December 8 and 9, 2010, the Geochemistry, Biogeochemistry, and Subsurface Science (GBSS) Science Theme Advisory Panel (STAP) convened for a more in-depth exploration of the five Science Theme focus areas developed at a similar meeting held in 2009. The goal for the fiscal year (FY) 2011 meeting was to identify potential topical areas for science campaigns, necessary experimental development needs, and scientific members for potential research teams. After a review of the current science in each of the five focus areas, the 2010 STAP discussions successfully led to the identification of one well focused campaign idea in pore-scale modeling and five longer-term potential research campaign ideas that would likely require additional workshops to identify specific research thrusts. These five campaign areas can be grouped into two categories: (1) the application of advanced high-resolution, high mass accuracy experimental techniques to elucidate the interplay between geochemistry and microbial communities in terrestrial ecosystems and (2) coupled computation/experimental investigations of the electron transfer reactions either between mineral surfaces and outer membranes of microbial cells or between the outer and inner membranes of microbial cells

Dengue Virus Infection Perturbs Lipid Homeostasis in Infected Mosquito Cells

Dengue virus causes ∼50–100 million infections per year and thus is considered one of the most aggressive arthropod-borne human pathogen worldwide. During its replication, dengue virus induces dramatic alterations in the intracellular membranes of infected cells. This phenomenon is observed both in human and vector-derived cells. Using high-resolution mass spectrometry of mosquito cells, we show that this membrane remodeling is directly linked to a unique lipid repertoire induced by dengue virus infection. Specifically, 15% of the metabolites detected were significantly different between DENV infected and uninfected cells while 85% of the metabolites detected were significantly different in isolated replication complex membranes. Furthermore, we demonstrate that intracellular lipid redistribution induced by the inhibition of fatty acid synthase, the rate-limiting enzyme in lipid biosynthesis, is sufficient for cell survival but is inhibitory to dengue virus replication. Lipids that have the capacity to destabilize and change the curvature of membranes as well as lipids that change the permeability of membranes are enriched in dengue virus infected cells. Several sphingolipids and other bioactive signaling molecules that are involved in controlling membrane fusion, fission, and trafficking as well as molecules that influence cytoskeletal reorganization are also up regulated during dengue infection. These observations shed light on the emerging role of lipids in shaping the membrane and protein environments during viral infections and suggest membrane-organizing principles that may influence virus-induced intracellular membrane architecture