Wenfang Wu

Characterization of the physiology and cell-mineral interactions of the marine anoxygenic phototrophic Fe(II) oxidizer Rhodovulum iodosum--implications for Precambrian Fe(II) oxidation.

Anoxygenic phototrophic Fe(II)-oxidizing bacteria (photoferrotrophs) are suggested to have contributed to the deposition of banded iron formations (BIFs) from oxygen-poor seawater. However, most studies evaluating the contribution of photoferrotrophs to Precambrian Fe(II) oxidation have used freshwater and not marine strains. Therefore, we investigated the physiology and mineral products of Fe(II) oxidation by the marine photoferrotroph Rhodovulum iodosum. Poorly crystalline Fe(III) minerals formed initially and transformed to more crystalline goethite over time. During Fe(II) oxidation, cell surfaces were largely free of minerals. Instead, the minerals were co-localized with EPS suggesting that EPS plays a critical role in preventing cell encrustation, likely by binding Fe(III) and directing precipitation away from cell surfaces. Fe(II) oxidation rates increased with increasing initial Fe(II) concentration (0.43-4.07 mM) under a light intensity of 12 μmol quanta m(-2) s(-1). Rates also increased as light intensity increased (from 3 to 20 μmol quanta m(-2) s(-1)), while the addition of Si did not significantly change Fe(II) oxidation rates. These results elaborate on how the physical and chemical conditions present in the Precambrian ocean controlled the activity of marine photoferrotrophs and confirm the possibility that such microorganisms could have oxidized Fe(II), generating the primary Fe(III) minerals that were then deposited to some Precambrian BIFs.

Reduced Efficiency of Magnetotaxis in Magnetotactic Coccoid Bacteria in Higher than Geomagnetic Fields

Magnetotactic bacteria are microorganisms that orient and migrate along magnetic field lines. The classical model of polar magnetotaxis predicts that the field-parallel migration velocity of magnetotactic bacteria increases monotonically with the strength of an applied magnetic field. We here test this model experimentally on magnetotactic coccoid bacteria that swim along helical trajectories. It turns out that the contribution of the field-parallel migration velocity decreases with increasing field strength from 0.1 to 1.5 mT. This unexpected observation can be explained and reproduced in a mathematical model under the assumption that the magnetosome chain is inclined with respect to the flagellar propulsion axis. The magnetic disadvantage, however, becomes apparent only in stronger than geomagnetic fields, which suggests that magnetotaxis is optimized under geomagnetic field conditions. It is therefore not beneficial for these bacteria to increase their intracellular magnetic dipole moment beyond the value needed to overcome Brownian motion in geomagnetic field conditions.

Physiology, Fe(II) oxidation, and Fe mineral formation by a marine planktonic cyanobacterium grown under ferruginous conditions

Evidence for Fe(II) oxidation and deposition of Fe(III)-bearing minerals from anoxic or redox-stratified Precambrian oceans has received support from decades of sedimentological and geochemical investigation of Banded Iron Formations (BIF). While the exact mechanisms of Fe(II) oxidation remains equivocal, reaction with O2 in the marine water column, produced by cyanobacteria or early oxygenic phototrophs, was likely. In order to understand the role of cyanobacteria in the deposition of Fe(III) minerals to BIF, we must first know how planktonic marine cyanobacteria respond to ferruginous (anoxic and Fe(II)-rich) waters in terms of growth, Fe uptake and homeostasis, and Fe mineral formation. We therefore grew the common marine cyanobacterium Synechococcus PCC 7002 in closed bottles that began anoxic, and contained Fe(II) concentrations that span the range of possible concentrations in Precambrian seawater. These results, along with cell suspension experiments, indicate that Fe(II) is likely oxidized by this strain via chemical oxidation with oxygen produced during photosynthesis, and not via any direct enzymatic or photosynthetic pathway. Imaging of the cell-mineral aggregates with scanning electron microscopy (SEM) and confocal laser scanning microscopy (CLSM) are consistent with extracellular precipitation of Fe(III) (oxyhydr)oxide minerals, but that >10% of Fe(III) sorbs to cell surfaces rather than precipitating. Proteomic experiments support the role of reactive oxygen species (ROS) in Fe(II) toxicity to Synechococcus PCC 7002. The proteome expressed under low Fe conditions included multiple siderophore biosynthesis and siderophore and Fe transporter proteins, but most siderophores are not expressed during growth with Fe(II). These results provide a mechanistic and quantitative framework for evaluating the geochemical consequences of perhaps life’s greatest metabolic innovation, i.e. the evolution and activity of oxygenic photosynthesis, in ferruginous Precambrian oceans.

Iron Isotope Fractionation during Fe(II) Oxidation Mediated by the Oxygen-Producing Marine Cyanobacterium Synechococcus PCC 7002

In this study, we couple iron isotope analysis to microscopic and mineralogical investigation of iron speciation during circumneutral Fe(II) oxidation and Fe(III) precipitation with photosynthetically produced oxygen. In the presence of the cyanobacterium Synechococcus PCC 7002, aqueous Fe(II) (Fe(II)aq) is oxidized and precipitated as amorphous Fe(III) oxyhydroxide minerals (iron precipitates, Feppt), with distinct isotopic fractionation (ε56Fe) values determined from fitting the δ56Fe(II)aq (1.79‰ and 2.15‰) and the δ56Feppt (2.44‰ and 2.98‰) data trends from two replicate experiments. Additional Fe(II) and Fe(III) phases were detected using microscopy and chemical extractions and likely represent Fe(II) and Fe(III) sorbed to minerals and cells. The iron desorbed with sodium acetate (FeNaAc) yielded heavier δ56Fe compositions than Fe(II)aq. Modeling of the fractionation during Fe(III) sorption to cells and Fe(II) sorption to Feppt, combined with equilibration of sorbed iron and with Fe(II)aq using published fractionation factors, is consistent with our resulting δ56FeNaAc. The δ56Feppt data trend is inconsistent with complete equilibrium exchange with Fe(II)aq. Because of this and our detection of microbially excreted organics (e.g., exopolysaccharides) coating Feppt in our microscopic analysis, we suggest that electron and atom exchange is partially suppressed in this system by biologically produced organics. These results indicate that cyanobacteria influence the fate and composition of iron in sunlit environments via their role in Fe(II) oxidation through O2 production, the capacity of their cell surfaces to sorb iron, and the interaction of secreted organics with Fe(III) minerals.

Laboratory Simulation of an Iron(II)-rich Precambrian Marine Upwelling System to Explore the Growth of Photosynthetic Bacteria

A conventional concept for the deposition of some Precambrian Banded Iron Formations (BIF) proceeds on the assumption that ferrous iron [Fe(II)] upwelling from hydrothermal sources in the Precambrian ocean was oxidized by molecular oxygen [O2] produced by cyanobacteria. The oldest BIFs, deposited prior to the Great Oxidation Event (GOE) at about 2.4 billion years (Gy) ago, could have formed by direct oxidation of Fe(II) by anoxygenic photoferrotrophs under anoxic conditions. As a method for testing the geochemical and mineralogical patterns that develop under different biological scenarios, we designed a 40 cm long vertical flow-through column to simulate an anoxic Fe(II)-rich marine upwelling system representative of an ancient ocean on a lab scale. The cylinder was packed with a porous glass bead matrix to stabilize the geochemical gradients, and liquid samples for iron quantification could be taken throughout the water column. Dissolved oxygen was detected non-invasively via optodes from the outside. Results from biotic experiments that involved upwelling fluxes of Fe(II) from the bottom, a distinct light gradient from top, and cyanobacteria present in the water column, show clear evidence for the formation of Fe(III) mineral precipitates and development of a chemocline between Fe(II) and O2. This column allows us to test hypotheses for the formation of the BIFs by culturing cyanobacteria (and in the future photoferrotrophs) under simulated marine Precambrian conditions. Furthermore we hypothesize that our column concept allows for the simulation of various chemical and physical environments - including shallow marine or lacustrine sediments.

Oxic Fe(III) reduction could have generated Fe(II) in the photic zone of Precambrian seawater

Many marine Precambrian iron formations (IF) record deep anoxic seawater enriched in Fe(II) (i.e. ferruginous) overlain by mildly oxygenated surface water. This is reflected by iron-rich sediments forming in deep basins, and relatively iron-poor sediments forming in shallow, sunlit waters. Such an iron gradient is often interpreted as a redox interface where dissolved Fe(II) was oxidized and precipitated as Fe(III)-bearing minerals. As such, sedimentary iron enrichments are proxy to the progressive oxidation of the oceans through geological time. However, this interpretation is founded on the assumption that Fe(II) could not persist within an oxygenated water column. Here, we cultivated cyanobacteria in an illuminated column supplied with Fe(II)-rich seawater medium in a laboratory-scale analog of a continental margin supporting IF deposition. We first observed Fe(II) oxidation with oxygen, then biologically-mediated reduction of Fe(III) (oxyhydr)oxides, which maintained a pool of Fe(II) in the presence of oxygen. Such steady-state iron redox cycling may have maintained dissolved, and hence mobile Fe(II) in oxygenated seawater above ferruginous deep basins such as those inferred for many Precambrian IF.