Extracellular haem peroxidases mediate Mn(II) oxidation in a marine Roseobacter bacterium via superoxide production.
Manganese (Mn) oxides are among the strongest sorbents and oxidants in environmental systems. A number of biotic and abiotic pathways induce the oxidation of Mn(II) to Mn oxides. Here, we use a combination of proteomic analyses and activity assays, to identify the enzyme(s) responsible for extracellular superoxide-mediated Mn oxide formation by a bacterium within the ubiquitous Roseobacter clade. We show that animal haem peroxidases (AHPs) located on the outer membrane and within the secretome are responsible for Mn(II) oxidation. These novel peroxidases have previously been implicated in direct Mn(II) oxidation by phylogenetically diverse bacteria. Yet, we show that in this Roseobacter species, AHPs mediate Mn(II) oxidation not through a direct reaction but by producing superoxide and likely also by degrading hydrogen peroxide. These findings point to a eukaryotic-like oscillatory oxidative-peroxidative enzymatic cycle by these AHPs that leads to Mn oxide formation by this organism. AHP expression appears unaffected by Mn(II), yet the large energetic investment required to produce and secrete these enzymes points to an as yet unknown physiological function. These findings are further evidence that bacterial peroxidases and secreted enzymes, in general, are unappreciated controls on the cycling of metals and reactive oxygen species (ROS), and by extension carbon, in natural systems.
Marine Chemistry and Geochemistry Department, Woods Hole Oceanographic Institution, 266 Woods Hole Rd MS# 52, Woods Hole, MA, 02543, USA.
Peter F
PF
Andeer
Department of Biology, Earth and Atmospheric Science, 190 Brooks Hall, Mt. Pleasant, MI, 48859, USA.
Deric R
DR
Learman
Marine Chemistry and Geochemistry Department, Woods Hole Oceanographic Institution, 266 Woods Hole Rd MS# 52, Woods Hole, MA, 02543, USA.
Matt
M
McIlvin
Department of Biology, Earth and Atmospheric Science, 190 Brooks Hall, Mt. Pleasant, MI, 48859, USA.
James A
JA
Dunn
Marine Chemistry and Geochemistry Department, Woods Hole Oceanographic Institution, 266 Woods Hole Rd MS# 52, Woods Hole, MA, 02543, USA.
Colleen M
CM
Hansel
D000818:Animals; D002244:Carbon / Q000737:chemistry; D006418:Heme / Q000378:metabolism*; D006861:Hydrogen Peroxide / Q000737:chemistry; D008345:Manganese / Q000737:chemistry*; D017895:Manganese Compounds / Q000737:chemistry; D010084:Oxidation-Reduction; D010087:Oxides / Q000737:chemistry; D010544:Peroxidases / Q000235:genetics / Q000378:metabolism*; D010802:Phylogeny; D040901:Proteomics; D041904:Roseobacter / Q000235:genetics / Q000378:metabolism*; D013481:Superoxides / Q000378:metabolism*
D017895:Manganese Compounds; D010087:Oxides; D013481:Superoxides; D006418:Heme; D008345:Manganese; C027424:manganese oxide; D002244:Carbon; D006861:Hydrogen Peroxide; D010544:Peroxidases