Biogeochemistry of Fe(II) oxidation in a photosynthetic microbial mat: Implications for Precambrian Fe(II) oxidation (original) (raw)
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FEMS Microbiology Ecology, 2014
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 lmol quanta m À2 s À1. Rates also increased as light intensity increased (from 3 to 20 lmol quanta m À2 s À1), 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.
Modulation of oxygen production in Archaean oceans by episodes of Fe(II) toxicity
Nature Geoscience, 2015
Oxygen accumulated in the surface waters of the Earth's oceans 1 and atmosphere 2 several hundred million years before the Great Oxidation Event between 2.4 and 2.3 billion years ago 3 . Before the Great Oxidation Event, periods of enhanced submarine volcanism associated with mantle plume events 4 supplied Fe(II) to sea water. These periods generally coincide with the disappearance of indicators of the presence of molecular oxygen in Archaean sedimentary records 5 . The presence of Fe(II) in the water column can lead to oxidative stress in some organisms as a result of reactions between Fe(II) and oxygen that produce reactive oxygen species 6 . Here we test the hypothesis that the upwelling of Fe(II)-rich, anoxic water into the photic zone during the late Archaean subjected oxygenic phototrophic bacteria to Fe(II) toxicity. In laboratory experiments, we found that supplying Fe(II) to the anoxic growth medium housing a common species of planktonic cyanobacteria decreased both the e ciency of oxygenic photosynthesis and their growth rates. We suggest that this occurs because of increasing intracellular concentrations of reactive oxygen species. We use geochemical modelling to show that Fe(II) toxicity in conditions found in the late Archaean photic zone could have substantially inhibited water column oxygen production, thus decreasing fluxes of oxygen to the atmosphere. We therefore propose that the timing of atmospheric oxygenation was controlled by the timing of submarine, plumetype volcanism, with Fe(II) toxicity as the modulating factor.
Frontiers in Earth Science, 2015
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 O 2 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.
Geobiology, 2005
During deposition of late Archean-early Palaeoproterozoic Precambrian banded iron formations (BIFs) the downward flux of ferric hydroxide (Fe(OH) 3 ) and phytoplankton biomass should have facilitated microbial Fe(III) reduction. However, quantifying the significance of such a metabolic pathway in the Precambrian is extremely difficult, considering the post-depositional alteration of the rocks and the lack of ideal modern analogues. Consequently, we have very few constraints on the Fe cycle at that time, namely (i) the concentration of dissolved Fe(II) in the ocean waters; (ii) by what mechanisms Fe(II) was oxidized (chemical, photochemical or biological, the latter using either O 2 or light); (iii) where the ferric hydroxide was precipitated (over the shelf vs. open ocean); (iv) the amount of phytoplankton biomass, which relates to the nutrient status of the surface waters; (v) the relative importance of Fe(III) reduction vs. the other types of metabolic pathways utilized by sea floor microbial communities; and (vi) the proportion of primary vs. diagenetic Fe(II) in BIF. Furthermore, although estimates can be made regarding the quantity of reducing equivalents necessary to account for the diagenetic Fe(II) component in Fe-rich BIF layers, those same estimates do not offer any insights into the magnitude of Fe(III) actually generated within the water column, and hence, the efficiency of Fe and C recycling prior to burial. Accordingly, in this study, we have attempted to model the ancient Fe cycle, based simply on conservative experimental rates of photosynthetic Fe(II) oxidation in the euphotic zone. We estimate here that under ideal growth conditions, as much as 70% of the biologically formed Fe(III) could have been recycled back into the water column via fermentation and organic carbon oxidation coupled to microbial Fe(III) reduction. By comparing the potential amount of biomass generated phototrophically with the reducing equivalents required for Fe(III) reduction and magnetite formation, we also hypothesize that another anaerobic metabolic pathway might have been utilized in the surface sediment to oxidize the fermentation by-products. Based on the premise that the deep ocean waters were anoxic, this role could have been fulfilled by methanogens, and maybe even methanotrophs that employed Fe(III) reduction.
Phototrophic Fe(II)-oxidation in the chemocline of a ferruginous meromictic lake
Frontiers in Microbiology, 2014
Precambrian Banded Iron Formation (BIF) deposition was conventionally attributed to the precipitation of iron-oxides resulting from the abiotic reaction of ferrous iron (Fe(II)) with photosynthetically produced oxygen. Earliest traces of oxygen date from 2.7 Ga, thus raising questions as to what may have caused BIF precipitation before oxygenic photosynthesis evolved. The discovery of anoxygenic phototrophic bacteria thriving through the oxidation of Fe(II) has provided support for a biological origin for some BIFs, but despite reports suggesting that anoxygenic phototrophs may oxidize Fe(II) in the environment, a model ecosystem of an ancient ocean where they are demonstrably active was lacking. Here we show that anoxygenic phototrophic bacteria contribute to Fe(II) oxidation in the water column of the ferruginous sulfate-poor, meromictic lake La Cruz (Spain). We observed in-situ photoferrotrophic activity through stimulation of phototrophic carbon uptake in the presence of Fe(II), and determined light-dependent Fe(II)-oxidation by the natural chemocline microbiota. Moreover, a photoferrotrophic bacterium most closely related to Chlorobium ferrooxidans was enriched from the ferruginous water column. Our study for the first time demonstrates a direct link between anoxygenic photoferrotrophy and the anoxic precipitation of Fe(III)-oxides in a ferruginous water column, providing a plausible mechanism for the bacterial origin of BIFs before the advent of free oxygen. However, photoferrotrophs represent only a minor fraction of the anoxygenic phototrophic community with the majority apparently thriving by sulfur cycling, despite the very low sulfur content in the ferruginous chemocline of Lake La Cruz.
Formation of Fe(III)-minerals by Fe(II)-oxidizing photoautotrophic bacteria
Geochimica et Cosmochimica Acta, 2004
It has been suggested that Fe(II)-oxidizing photoautotrophic bacteria may have catalyzed the precipitation of an ancient class of sedimentary deposits known as Banded Iron Formations. In order to evaluate this claim, it is necessary to define and understand this process at a molecular level so that putative Fe-isotope "biosignatures" in ancient rocks can be interpreted. In this report, we characterize the substrates and products of photoautotrophic Fe(II)-oxidation by three phylogenetically distinct Fe(II)-oxidizing bacteria. In every case, dissolved Fe(II) is used as the substrate for oxidation, and there is no evidence for active dissolution of poorly soluble Fe(II)-minerals by biogenic organic ligands. Poorly crystalline Fe(III) (hydr)oxide mineral phases are initially precipitated, and as they age, rapidly convert to the crystalline minerals goethite and lepidocrocite. Although the precipitates appear to associate with the cell wall, they do not cover it entirely, and precipitate-free cells represent a significant portion of the population in aged cultures. Citrate is occasionally detected at nanomolar concentrations in all culture fluids, whereas an unknown organic molecule is always present in two out of the three bacterial cultures. Whether these molecules are released by the cell to bind Fe(III) and prevent the cell from encrustation by Fe(III) (hydr)oxides is uncertain, but seems unlikely if we assume Fe(II)-oxidation occurs at the cell surface. In light of the energetic requirement the cell would face to produce ligands for this purpose, and given the local acidity metabolically generated in the microenvironment surrounding Fe(II)-oxidizing cells, our results suggest that Fe(III) is released in a dissolved form as an inorganic aqueous complex and/or as a colloidal aggregate prior to mineral precipitation. The implication of these results for the interpretation of Fe-isotope fractionation measured for this class of bacteria is that equilibrium processes involving free biological ligands do not account for the observed fractionation.
Deposition of banded iron formations by anoxygenic phototrophic Fe(II)-oxidizing bacteria
Geology, 2005
Figure 1. Wavelength-dependent light intensity at different water depths (indicated by numbers assigned to contour lines). Light intensity is given in percent of surface light intensity, where 100% equals~30,000 lux (~600 mol quanta m ؊2 s ؊1 ), estimated to be 24 h average expected for light intensity on horizontal surface on clear summer day (Thimijan and Heins, 1983). Contour lines were derived using attenuation coefficients given for clear ocean water by Smith and Baker (1981). Dashed lines represent light intensities at 25 and 100 m depth, respectively, including absorption by 25 and 100 m water column and 17.6-m-thick layer of anoxygenic phototrophic Fe(II) oxidizers containing 10 6 cells/mL. Shaded area indicates wavelength region where carotenoids absorb light.