Mn(II) oxidation by an ascomycete fungus is linked to superoxide production during asexual reproduction

Abstract

Manganese (Mn) oxides are among the most reactive minerals within the environment, where they control the bioavailability of carbon, nutrients, and numerous metals. Although the ability of microorganisms to oxidize Mn(II) to Mn(III/IV) oxides is scattered throughout the bacterial and fungal domains of life, the mechanism and physiological basis for Mn(II) oxidation remains an enigma. Here, we use a combination of compound-specific chemical assays, microspectroscopy, and electron microscopy to show that a common Ascomycete filamentous fungus, Stilbella aciculosa , oxidizes Mn(II) to Mn oxides by producing extracellular superoxide during cell differentiation. The reactive Mn oxide phase birnessite and the reactive oxygen species superoxide and hydrogen peroxide are colocalized at the base of asexual reproductive structures. Mn oxide formation is not observed in the presence of superoxide scavengers (e.g., Cu) and inhibitors of NADPH oxidases (e.g., diphenylene iodonium chloride), enzymes responsible for superoxide production and cell differentiation in fungi. Considering the recent identification of Mn(II) oxidation by NADH oxidase-based superoxide production by a common marine bacterium ( Roseobacter sp.), these results introduce a surprising homology between some prokaryotic and eukaryotic organisms in the mechanisms responsible for Mn(II) oxidation, where oxidation appears to be a side reaction of extracellular superoxide production. Given the versatility of superoxide as a redox reactant and the widespread ability of fungi to produce superoxide, this microbial extracellular superoxide production may play a central role in the cycling and bioavailability of metals (e.g., Hg, Fe, Mn) and carbon in natural systems.

Superoxide-Mediated Extracellular Biosynthesis of Silver Nanoparticles by the Fungus Fusarium oxysporum

“…It was reported that superoxide can be produced by bacteria and fungi. [19][20][21]23,24 Here, for the first time, we demonstrated the production of superoxide by F. oxysporum by using continuous flow CL (Figure 2). No CL signal was observed when only F.…”

“…46,47 Here we discovered superoxide plays a crucial role in the extracellular synthesis of AgNPs by the fungus F. oxysporum. As superoxide is widely produced in bacteria, 19 fungi, 20 algae, 48 and plants, 49 this study is helpful for understanding the mechanism of AgNP biosynthesis, which will have great implications for the enhancement of AgNP synthesis in the future. In addition, this study also improves our understanding of biomineralization of silver and the source of naturally occurring AgNPs.…”

“…As the antibacterial activities of AgNPs are much lower than that of Ag + , 50 this bioreduction is also a possible natural antidote to mitigate the toxicity of silver to organisms. Considering the key roles of superoxide in the redox cycles of Fe, 23,51 Mn, 20,21 Cu, 32,52,53 Cr, 54,55 As, 56,57 and I, 22 it is expected that the superoxide-produced organisms should also have great impacts on the biogeochemical cycles of these elements. …”

“…Cu 2+ is an effective and rapid superoxide scavenger, while chemically similar Zn 2+ cannot catalyze the dismutation of superoxide. 20,21,31 The effect of Cu 2+ (as a superoxide scavenger) and Zn 2+ (as a control) on the formation of AgNPs by F. oxysporum was therefore investigated ( Figure 3A). The addition of Cu 2+ can induce a concentration-dependent inhibition of AgNP formation, suggesting a critical role of superoxide as the reductant of Ag + .…”

“…Recently, it has been demonstrated that bacteria and fungi can produce superoxide, 19,20 which can further mediate the oxidation of Mn(II) 20,21 and I − , 22 and the reduction of Fe(III). 23,24 As demonstrated previously, superoxide produced from KO 2 25,26 or photoirradiated natural organic matter 27 can also reduce Ag + into AgNPs.…”