Manganese(II)-oxidizing Ascomycete fungi experience growth benefit on polyphenolic substrate

The ability of micro-organisms to oxidize manganese (Mn)(II) to Mn(III) is a strong predictor of litter decomposition rates in soils. While white rot Basidiomycete fungi generate reactive Mn(III) to degrade lignin, it remains unclear whether Mn(II) oxidation may provide a physiological benefit to litter-degrading filamentous Ascomycete fungi. We grew 3 Mn(II)-oxidizing Ascomycetes on phenolic and non-phenolic substrates and evaluated growth, Mn(II) oxidation, and carbon (C) degradation. Extracellular Mn(II) oxidative capacity was inducible by Mn(II) in Stagonospora sp. SRC1lsM3a and Pyrenochaeta sp. DS3sAY3a, indicating an active rather than accidental process. Oxidative capacity was constitutively expressed in Paraconiothyrium sporulosum AP3s5-JAC2a. Compared to Mn-free controls, growth with Mn(II) increased hyphal extension rate in all 3 fungi (6.2%, 31%, and 5.1%, respectively) on minimal medium supplemented with 5 g/l of the polyphenolic substrate tannic acid (TA), but not on non-phenolic substrates. Mn(II) stimulated polyphenolic oxidative capacity in Stagonospora sp. and Pyrenochaeta sp., indicating a link between Mn and degradation of TA. This work suggests a homology between Ascomycete and Basidiomycete fungi in coupling Mn(II) oxidation to C oxidation, suggests a physiological role for Mn(II) oxidation in Ascomycetes, and increases our understanding of how micro-organisms regulate Mn redox cycling and litter decomposition in soils.