Biosignatures link microorganisms to iron mineralization in a paleoaquifer (original) (raw)
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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.
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.
Frontiers in microbiology, 2014
The Cambrian-age Mt. Simon Sandstone, deeply buried within the Illinois Basin of the midcontinent of North America, contains quartz sand grains ubiquitously encrusted with iron-oxide cements and dissolved ferrous iron in pore-water. Although microbial iron reduction has previously been documented in the deep terrestrial subsurface, the potential for diagenetic mineral cementation to drive microbial activity has not been well studied. In this study, two subsurface formation water samples were collected at 1.72 and 2.02 km, respectively, from the Mt. Simon Sandstone in Decatur, Illinois. Low-diversity microbial communities were detected from both horizons and were dominated by Halanaerobiales of Phylum Firmicutes. Iron-reducing enrichment cultures fed with ferric citrate were successfully established using the formation water. Phylogenetic classification identified the enriched species to be related to Vulcanibacillus from the 1.72 km depth sample, while Orenia dominated the communiti...
Characterisation of iron oxide encrusted microbial fossils
Scientific Reports
Robust methods for the characterisation of microbial biosignatures in geological matrices is critical for developing mineralogical biosignatures. Studying microbial fossils is fundamental for our understanding of the role microorganisms have played in elemental cycling in modern and ancient environments on Earth and potentially Mars. Here, we aim to understand what promotes the fossilisation of microorganisms after the initial stages of biomineralisation, committing bacteriomorphic structures to the geological record within iron-rich environments. Mineral encrusted cell envelope structures were routinely identified within a goethite-rich vein that cross-cut the saprolite (iron ore) of a weathered banded iron formation (BIF) system in the Quadrilátero Ferrífero, Brazil. The preservation of potential organic and mineralogical biosignatures associated with these fossils was characterised using the following high-resolution analytical techniques: scanning and transmission electron micro...
Microbial mediated formation of Fe-carbonate minerals under extreme acidic conditions
Scientific Reports, 2014
Discovery of Fe-carbonate precipitation in Rio Tinto, a shallow river with very acidic waters, situated in Huelva, South-western Spain, adds a new dimension to our understanding of carbonate formation. Sediment samples from this low-pH system indicate that carbonates are formed in physico-chemical conditions ranging from acid to neutral pH. Evidence for microbial mediation is observed in secondary electron images , which reveal rod-shaped bacteria embedded in the surface of siderite nanocrystals. The formation of carbonates in Rio Tinto is related to the microbial reduction of ferric iron coupled to the oxidation of organic compounds. Herein, we demonstrate for the first time, that Acidiphilium sp. PM, an iron-reducing bacterium isolated from Rio Tinto, mediates the precipitation of siderite (FeCO 3 ) under acidic conditions and at a low temperature (306C). We describe nucleation of siderite on nanoglobules in intimate association with the bacteria cell surface. This study has major implications for understanding carbonate formation on the ancient Earth or extraterrestrial planets. I n the geologic record, evidence for the existence of microorganisms has been observed in sedimentary rocks as old as 3.45 Ga, and their influence on mineral precipitation throughout Earth's history, particularly for carbonate deposits, has been and remains significant 1,2 . However, thermodynamic conditions fundamentally restrict carbonate precipitation to high pH environments (pH . 7), and, in terrestrial environments, the production of carbonates at pH , 4.5 does not occur either by abiotic or biotic mechanisms 3-5 . In spite of this general rule, Fe-rich carbonate minerals have been recently recognized in the subsurface of Rio Tinto in mildly acidic to neutral pH (5-7) and somewhat reducing (Eh , 0) conditions 6,7 . Rio Tinto is an acid-sulphate system considered as one of the potential analogues for life on early Earth and Mars 7 . Acidiphilium species are very abundant in Rio Tinto 8 , these alphaproteobacteria can grow on organic compounds under microaerobiosis and anaerobic conditions using ferric iron (Fe 31 ) and/or oxygen as electron acceptors 9,10 . In this study, we conducted culture experiments with Acidiphilium species to investigate the mediation of carbonate precipitation under low pH and temperature conditions. We present a high-resolution transmission electron microscopy (TEM), atomic force microscopy (AFM), scanning electron microscopy (SEM) and Raman spectroscopy study of the microbial carbonate precipitates (see methods section). We propose that the direct mediation of acidophilic microorganisms can overcome kinetic barriers to carbonate formation and that they may play an active role in the formation of carbonates in acidic and natural environments.
Geochimica et Cosmochimica Acta, 2007
We studied the role of microbial photosynthesis in the oxidation of Fe(II) to Fe(III) in a high Fe(II) and high Mn(II) hot spring devoid of sulfide and atmospheric oxygen in the source waters. In situ light and dark microelectrode measurements of Fe(II), Mn(II) and O 2 were made in the microbial mat consisting of cyanobacteria and anoxygenic photosynthetic Chloroflexus sp. We show that Fe(II) oxidation occurred when the mat was exposed to varying intensities of sunlight but not near infrared light. We did not observe any Mn(II) oxidation under any light or dark condition over the pH range 5-7. We observed the impact of oxygenic photosynthesis on Fe(II) oxidation, distinct from the influence of atmospheric O 2 and anoxygenic photosynthesis. In situ Fe(II) oxidation rates in the mats and cell suspensions exposed to light are consistent with abiotic oxidation by O 2 . The oxidation of Fe(II) to form primary Fe(III) phases contributed to banded iron-formations (BIFs) during the Precambrian. Both oxygenic photosynthesis, which produces O 2 as an oxidizing waste product, and anoxygenic photosynthesis in which Fe(II) is used to fix CO 2 have been proposed as Fe(II) oxidation mechanisms. Although we do not know the specific mechanisms responsible for all Precambrian Fe(II) oxidation, we assessed the relative importance of both mechanisms in this modern hot spring environment. In this environment, cyanobacterial oxygen production accounted for all the observed Fe(II) oxidation. The rate data indicate that a modest population of cyanobacteria could have mediated sufficient Fe(II) oxidation for some BIFs.
Biogeochemical transformation of Fe minerals in a petroleum-contaminated aquifer
Geochimica et Cosmochimica Acta, 2004
The Bemidji aquifer in Minnesota, USA is a well-studied site of subsurface petroleum contamination. The site contains an anoxic groundwater plume where soluble petroleum constituents serve as an energy source for a region of methanogenesis near the source and bacterial Fe(III) reduction further down gradient. Methanogenesis apparently begins when bioavailable Fe(III) is exhausted within the sediment. Past studies indicate that Geobacter species and Geothrix fermentens-like organisms are the primary dissimilatory Fe-reducing bacteria at this site. The Fe mineralogy of the pristine aquifer sediments and samples from the methanogenic (source) and Fe(III) reducing zones were characterized in this study to identify microbiologic changes to Fe valence and mineral distribution, and to identify whether new biogenic mineral phases had formed. Methods applied included X-ray diffraction; X-ray fluorescence (XRF); and chemical extraction; optical, transmission, and scanning electron microscopy; and Mössbauer spectroscopy. All of the sediments were low in total Fe content (Ϸ 1%) and exhibited complex Fe-mineralogy. The bulk pristine sediment and its sand, silt, and clay-sized fractions were studied in detail. The pristine sediments contained Fe(II) and Fe(III) mineral phases. Ferrous iron represented approximately 50% of Fe TOT. The relative Fe(II) concentration increased in the sand fraction, and its primary mineralogic residence was clinochlore with minor concentrations found as a ferroan calcite grain cement in carbonate lithic fragments. Fe(III) existed in silicates (epidote, clinochlore, muscovite) and Fe(III) oxides of detrital and authigenic origin. The detrital Fe(III) oxides included hematite and goethite in the form of mm-sized nodular concretions and smaller-sized dispersed crystallites, and euhedral magnetite grains. Authigenic Fe(III) oxides increased in concentration with decreasing particle size through the silt and clay fraction. Chemical extraction and Mössbauer analysis indicated that this was a ferrihydrite like-phase. Quantitative mineralogic and Fe(II/III) ratio comparisons between the pristine and contaminated sediments were not possible because of textural differences. However, comparisons between the texturally-similar source (where bioavailable Fe(III) had been exhausted) and Fe(III) reducing zone sediments (where bioavailable Fe(III) remained) indicated that dispersed detrital, crystalline Fe(III) oxides and a portion of the authigenic, poorly crystalline Fe(III) oxide fraction had been depleted from the source zone sediment by microbiologic activity. Little or no effect of microbiologic activity was observed on silicate Fe(III). The presence of residual "ferrihydrite" in the most bioreduced, anoxic plume sediment (source) implied that a portion of the authigenic Fe(III) oxides were biologically inaccessible in weathered, lithic fragment interiors. Little evidence was found for the modern biogenesis of authigenic ferrous-containing mineral phases, perhaps with the exception of thin siderite or ferroan calcite surface precipitates on carbonate lithic fragments within source zone sediments.
Journal of Arid Environments, 2013
Previous work showed the cryptoendolithic microbial communities of the Colorado Plateau act to harden the surfaces of Jurassic Navajo Sandstone outcrops via the production of extracellular polymeric substances (EPS). It is our hypothesis that EPS produced in these systems serve to trap ions and maintain hydration. EPS isolated from in vitro and in vivo biofilms bind 200e600 nmol of ferrous iron per 10 g of biofilm sample. Initial characterizations of the EPS used preparations from two distinct microbial cultures grown in semi-submerged conditions with EPS harvested from approximately one-half of each culture immediately, the remaining biofilm was allowed to dry before the EPS was harvested. Analysis of ferrous iron binding of the four preparations showed that the culture dominated with non-filamentous cells only produced a chelating moiety after desiccation. Conversely, the second culture dominated by filamentous cells produced a ferrous iron binding activity when semi-submerged. Biochemical characterization showed that the extracted EPS was acidic, containing 37% uronic acid. Neither the EPS nor the biofilms had the ability to retain water though an increase in the rate of water loss was noted. We conclude that EPS produced by these communities are involved in nutrient capture as well as stabilization.