Abstract

Manganese (Mn) oxide minerals influence the availability of organic carbon, nutrients and metals in the environment. Oxidation of Mn(II) to Mn(III/IV) oxides is largely promoted by the direct and indirect activity of microorganisms. Studies of biogenic Mn(II) oxidation have focused on bacteria and fungi, with phototrophic organisms (phototrophs) being generally overlooked. Here, we isolated phototrophs from Mn removal beds in Pennsylvania, USA, including fourteen Chlorophyta (green algae), three Bacillariophyta (diatoms) and one cyanobacterium, all of which consistently formed Mn(III/IV) oxides. Isolates produced cell-specific oxides (coating some cells but not others), diffuse biofilm oxides, and internal diatom-specific Mn-rich nodules. Phototrophic Mn(II) oxidation had been previously attributed to abiotic oxidation mediated by photosynthesis-driven pH increases, but we found a decoupling of Mn oxide formation and pH alteration in several cases. Furthermore, cell-free filtrates of some isolates produced Mn oxides at specific time points, but this activity was not induced by Mn(II). Manganese oxide formation in cell-free filtrates occurred via reaction with the oxygen radical superoxide produced by soluble extracellular proteins. Given the known widespread ability of phototrophs to produce superoxide, the contribution of phototrophs to Mn(II) oxidation in the environment may be greater and more nuanced than previously thought.

Highlights

  • Manganese (Mn) oxide minerals influence the availability of organic carbon, nutrients and metals in the environment

  • Drill cores through an early Paleoproterozoic succession (2.415 Ga) contain Mn enrichment that predates the rise of molecular oxygen, suggesting that the oxygen-evolving complex of photosystem II (PSII) arose from an earlier photosystem that carried out single-electron oxidation of Mn and formed Mn oxide minerals rather than O243,44

  • We found that Mn oxide formation activity was widespread among phototrophs isolated from two manganese removal beds (MRBs) treating coal mine drainage in western Pennsylvania, De Sale Phases 1 and 2 (DS1 and DS2, respectively)

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Summary

Introduction

Manganese (Mn) oxide minerals influence the availability of organic carbon, nutrients and metals in the environment. Manganese (Mn) oxide minerals are ubiquitous in soils and sediments Due to their exceptional scavenging and redox capabilities, Mn oxides exert a disproportionately high influence on the availability and fate of organic carbon (e.g. lignin, humic acids), nutrients (e.g. phosphate) and metals (e.g. Pb, Zn, Co, Ni, As, Cr) in the environment[1,2,3,4,5]. The formation of these minerals can occur via abiotic pathways in systems with elevated pH6, but in most natural environments, it is thought to be induced by the direct and/or indirect activity of Mn(II)-oxidising microorganisms[3,7]. Mn oxidation lies at the heart of photosynthesis; it is directly responsible for most of Earth’s primary productivity, and at least partially responsible for the increase in free O2 in the atmosphere[42]

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