Fungi are the primary decomposers of dead plant material (i.e., litter) in terrestrial environments, controlling a major flux of carbon (C) between the biosphere and atmosphere. Recent studies have shown that litter decomposition on the forest floor is tightly coupled to the redox cycling of manganese (Mn) by soil fungi. While white-rot Basidiomycete fungi catalyze the oxidation of Mn(II) to reactive Mn(III) to aid in lignocellulose breakdown, it remains unclear whether Ascomycete fungi, which typically dominate litter-degrading communities, harness Mn(II) oxidation for lignocellulose degradation as well. Furthermore, a physiological role for Mn(II) oxidation in Ascomycete fungi has yet to be identified. We hypothesized that Mn(II) oxidation would confer a growth benefit to Ascomycetes when grown on recalcitrant C sources but not labile C sources, since reactive Mn(III) or Mn(III/IV) oxides might increase their access to recalcitrant C. To test this hypothesis, we grew three Mn(II)-oxidizing Ascomycetes (Stagonospora sp. SRC1lsM3a, Pyrenochaeta sp. DS3sAY3a, and Paraconiothyrium sporulosum AP3s5-JAC2a) on four C sources ranging from labile to recalcitrant, and we evaluated their hyphal extension rate with or without Mn(II) added to the medium. In addition, we qualitatively assessed their ability to produce Mn(III/IV) oxides on each C source and to degrade polyphenolic substrates.
Results/Conclusions
Our primary finding was that, in support of our hypothesis, all 3 Ascomycetes grew significantly faster (P<0.01) on recalcitrant C sources when supplemented with Mn(II) than without, and this growth benefit was lost on labile C sources. Growth rates on recalcitrant C increased by 5-10% in Stagonospora sp. and P. sporulosum and over 400% in Pyrenochaeta sp. Visible brown Mn oxides were not produced by any species, suggesting that these fungi may use the reactive intermediate Mn(III) to aid in growth on recalcitrant C instead of Mn(III/IV) oxide minerals. Finally, all 3 species were able to grow on tannic acid, a polyphenol similar to lignin, as their sole C source. Clearing zones surrounding the mycelia during growth suggest tannic acid degradation. Together, these results suggest that Ascomycetes may indeed harness Mn(II) oxidation to increase their access to recalcitrant C, similar to white-rot Basidiomycetes. Increased growth in the presence of Mn(II) suggests that Mn(II) oxidation confers a physiological benefit to these fungi on recalcitrant C. This work illustrates that Ascomycete fungi may be important contributors to Mn-linked lignocellulose degradation in the environment. We are currently validating these results by establishing a concentration dependence between Mn(II) concentration and fungal growth benefit.