Abstract
Manganese (Mn) oxides are among the strongest sorbents and oxidants within the environment, controlling the fate and transport of numerous elements and the degradation of recalcitrant carbon. Both bacteria and fungi mediate the oxidation of Mn(II) to Mn(III/IV) oxides but the genetic and biochemical mechanisms responsible remain poorly understood. Furthermore, the physiological basis for microbial Mn(II) oxidation remains an enigma. We have recently reported that a common marine bacterium (Roseobacter sp. AzwK-3b) oxidizes Mn(II) via reaction with extracellular superoxide (O (sub 2) (super -) ) produced during exponential growth [1]. Here we expand this superoxide-mediated Mn(II) oxidation pathway to fungi, introducing a surprising homology between prokaryotic and eukaryotic metal redox processes. For instance, Stilbella aciculosa, a common soil Ascomycete filamentous fungus, precipitates Mn oxides at the base of asexual reproductive structures. This distribution is a consequence of localized production of superoxide by the well-known NADPH oxidase enzymes, leading to abiotic oxidation of Mn(II) by superoxide. Disruption of NADPH oxidase activity using the common oxidoreductase inhibitor DPI leads to diminished cell differentiation and subsequent Mn(II) oxidation inhibition. We also show here that similar to fungi extracellular superoxide production is widespread throughout the bacterial domain. Yet, superoxide production does not, in fact, confer the ability to produce Mn oxides. This is a consequence of a backreaction between the products (Mn(III) and hydrogen peroxide) formed upon Mn(II) and superoxide reaction, leading to the regeneration of Mn(II). Indeed, we show that superoxide-mediated Mn oxide formation is reliant upon the removal of the hydrogen peroxide product. Thus, the formation of Mn oxides by the Roseobacter and Stilbella spp. requires both the production of superoxide and consumption of hydrogen peroxide. We believe that this need for hydrogen peroxide consumption hints to the role of heme peroxidases (recently implicated Mn oxidases) in bacterial Mn oxidation. Taking into consideration that superoxide is a strong and versatile redox reactant serving as both an oxidant (e.g., Mn) and reductant (e.g., Fe, Cu, Hg) of metals, biological superoxide production may have profound influences on metal biogeochemistry beyond Mn.