Mn oxide formation by phototrophs: Spatial and temporal patterns, with evidence of an enzymatic superoxide-mediated pathway

Dominique L. Chaput, Alexandré J. Fowler, Onyou Seo, Kelly Duhn, Colleen M. Hansel, Cara M. Santelli

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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.

Original languageEnglish (US)
Article number18244
JournalScientific reports
Issue number1
StatePublished - Dec 1 2019

Bibliographical note

Funding Information:
This work was funded by a Smithsonian Scholarly Studies grant to CMS, by a Smithsonian Postdoctoral Fellowship to DLC, by the National Science Foundation, grant number CBET-1336496, to CMH and CMS, and by MnDRIVE Environment at the University of Minnesota to CMS. We thank Margaret Dunn and Cliff Denholm, Stream Restoration Inc., for assistance and access to field sites, Carolyn Zeiner (WHOI/Harvard) for useful discussions and advice regarding ROS experiments, as well as Jeff Post, Tim Rose and Tim Gooding (Smithsonian NMNH) for assistance with the SEM/EDS work. Portions of the laboratory work were conducted in and with the support of the L.A.B. facilities at the National Museum of Natural History, Smithsonian Institution.


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