Colloquium: Colleen Hansel

Colleen Hansel, Associate Scientist, "Marine Chemistry & Geochemistry, Woods Hole Oceanographic Institution

Abstract: The oxidized manganese (Mn) species, Mn³⁺ and Mn⁴⁺, are among the strongest natural oxidants on our planet possessing the rare ability to oxidize recalcitrant inorganic (e.g., Cr³⁺) and organic (e.g., humics) compounds. 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, as energy is not conserved in this process, the physiological basis for bacterial Mn(II) oxidation remains an enigma. We have recently revealed that Mn oxide formation by some fungal and bacterial species is a consequence of Mn(II) oxidation by the reactive oxygen species (ROS) superoxide (O₂^-). This superoxide production is formed extracellularly, in some cases through the activity of transmembrane and secreted proteins (exoproteins). The enzymes responsible for superoxide production by some marine bacteria are heme peroxidases that are secreted from the cell in high abundance but not induced by the presence of manganese. While we have also shown that extracellular superoxide production is widespread in bacteria, this production does not in fact confer the ability to produce Mn oxides.  Indeed, back-reaction between the products, Mn(III) and hydrogen peroxide, formed upon Mn(II) and superoxide reaction inhibits Mn oxide formation. Within abiotic systems, we show that superoxide-mediated Mn oxide formation is reliant upon the removal of the hydrogen peroxide product. These findings indicate that at least two processes – the generation of superoxide and consumption of hydrogen peroxide – are requisite for Mn oxide formation. This thereby points to a dual role for heme peroxidases in bacterial Mn(II) oxidation, where these enzymes possess a peroxidative-oxidative oscillatory behavior as is widely observed in eukaryotic peroxidases, but not yet appreciated in prokaryotic systems. ROS and Mn cycling may be tightly coupled in natural systems, wherein the production and consumption of superoxide and hydrogen peroxide could be mediated by the recycling of catalytic levels of aqueous Mn – a so-called cryptic Mn cycle.  In this way, Mn may in fact be the antioxidant of the ocean – and quite possibly the primordial superoxide dismutase.