Use of Superoxide as an Electron Shuttle for Iron Acquisition by the Marine Cyanobacterium Lyngbya majuscula

Abstract

Reduction of iron from the ferric state to the ferrous state is one strategy employed by microorganisms in nearneutral environments to increase its biological availability. In recent years, the existence of mobile reducing agents produced bymicroorganismsto promote iron reduction, known as electron shuttles, has been demonstrated. Production of electron shuttles has been shown for several organisms, employing a variety of mostly organic molecules as the electron carrier. Here we show that the coastal cyanobacterium Lyngbya majuscula produces iron-reducing superoxide radicals (02*-) and that this facilitates increased iron uptake. We suggest that superoxide is a useful electron shuttle because it reacts rapidly and almost indiscriminately with Fe(lll)-organic complexes and its precursor, dissolved oxygen, is ubiquitous in the photic zone. We further suggest that, for these reasons, the generation of superoxide by marine oxygenic photosynthetic microorganisms and its use in facilitating iron uptake may be a reasonably widespread process.

Effects of nutrients, salinity, pH and light:dark cycle on the production of reactive oxygen species in the alga Chattonella marina

“…The other major ROS sources in photosynthetic organisms are certain enzymatic systems (Halliwell and Gutteridge, 1999), and results of Western blotting using antibody raised against the human neutrophil cytochrome b558 large subunit (gp91phox, a sub-unit of NADPH oxidase) showed that C. marina generates ROS possibly through a plasma membrane NADPH-dependent enzymatic pathway (Kim et al, 2000). Our experiments showed that ROS production was significantly enhanced upon addition of vitamin K 3 , while ROS production was inhibited by dicumarol ( Rose et al (2005) proposed that the marine cyanobacterium Lyngbya majuscula may use superoxide as an electron shuttle to reduce Fe(III) for iron uptake.…”

Mn(II) oxidation by an ascomycete fungus is linked to superoxide production during asexual reproduction

“…Indeed, oxidation of Mn(II) to Mn oxides by a common marine bacterium, Roseobacter AzwK-3b, was found to be a consequence of enzymatic extracellular production of O 2 − , which served as the terminal oxidant of Mn(II) (19). Although extracellular superoxide production has been documented in pathogenic bacteria (20) and phytoplankton (21), very little is known about the occurrence of this process in nonpathogenic heterotrophic bacteria. In contrast, production of extracellular superoxide is widespread throughout the fungal kingdom (22), where it is involved in host defense, posttranslational modification of proteins, hyphal branching, cell signaling, and cell differentiation (22,23).…”

Saccharides enhance iron bioavailability to Southern Ocean phytoplankton

“…S1), the mechanism(s) controlling iron bioavailability to oceanic biota remain poorly understood. Iron bioavailability is influenced by photochemistry (3), chemical speciation (4,5), biological cycling (6), and uptake strategies (7)(8)(9). As a result, different microorganisms, each with its own specific iron requirement, iron uptake system(s), and biological adaptability (7,10,11), will have access to different pools of bioavailable iron under conditions of identical iron chemistry.…”