In Situ Fe and S isotope analyses in pyrite from the 3.2 Ga Mendon Formation (Barberton Greenstone Belt, South Africa): Evidence for early microbial iron reduction

International audienceOn the basis of phylogenetic studies and laboratory cultures, it has been proposed that the ability of microbes to metabolize iron has emerged prior to the Archaea/ Bacteria split. However, no unambiguous geochemical data supporting this claim have been put forward in rocks older than 2.7-2.5 giga years (Gyr). In the present work, we report in situ Fe and S isotope composition of pyrite from 3.28-to 3.26-Gyr-old cherts from the upper Mendon Formation, South Africa. We identified three populations of microscopic pyrites showing a wide range of Fe isotope compositions, which cluster around two δ 56 Fe values of −1.8‰ and +1‰. These three pyrite groups can also be distinguished based on the pyrite crystallinity and the S isotope mass-independent signatures. One pyrite group displays poorly crystallized pyrite minerals with positive Δ 33 S values > +3‰, while the other groups display more variable and closer to 0‰ Δ 33 S values with recrystallized pyrite rims. It is worth to note that all the pyrite groups display positive Δ 33 S values in the pyrite core and similar trace element compositions

Investigating Microbe-Mineral Interactions: Recent Advances in X-Ray and Electron Microscopy and Redox-Sensitive Methods

International audienceMicrobe-mineral interactions occur in diverse modern environments, from the deep sea and subsurface rocks to soils and surface aquatic environments. They may have played a central role in the geochemical cycling of major (e.g., C, Fe, Ca, Mn, S, P) and trace (e.g., Ni, Mo, As, Cr) elements over Earth's history. Such interactions include electron transfer at the microbe-mineral interface that left traces in the rock record. Geomicrobiology consists in studying interactions at these organic-mineral interfaces in modern samples and looking for traces of past microbe-mineral interactions recorded in ancient rocks. Specific tools are required to probe these interfaces and to understand the mechanisms of interaction between microbes and minerals from the scale of the biofilm to the nanometer scale. In this review, we focus on recent advances in electron microscopy, in particular in cryoelectron microscopy, and on a panel of electrochemical and synchrotron-based methods that have recently provided new understanding and imaging of the microbe-mineral interface, ultimately opening new fields to be explored

Formation of pyrite spherules from mixtures of biogenic FeS and organic compounds during experimental diagenesis

International audiencePyrite (urn:x-wiley:15252027:media:ggge22649:ggge22649-math-0001) is the most common iron sulfide on the Earth's surface and has widely been used as a paleo-environmental proxy. Yet the information recorded by pyrite depends on whether it was formed through abiotic or biogenic routes. It is thus of importance to properly identify its origin. Here, we investigate the final morphology of pyrite produced upon a simulated diagenetic history from biogenic and abiotic iron sulfide/phosphate systems. Abiotic starting material obtained by chemical synthesis and biogenic starting material produced from pure culture of Desulfovibrio desulfuricans were submitted to increasing diagenetic conditions (75°C or 150°C from 1 to 10 days). Mineralogical products were characterized by X-ray diffraction and electron microscopy. For both biogenic and abiotic starting materials, the final state was characterized by the association of pyrite and lipscombite (urn:x-wiley:15252027:media:ggge22649:ggge22649-math-0002), the most stable phases in these conditions. Intermediate phases such as greigite for iron sulfides and beraunite/wolfeite for iron phosphates were present in the abiotic residue but were not detected in the biogenic residue. Distinct pyrite morphologies were observed depending on the presence of organic matter. Indeed, while abiotic starting material led to the formation of submicrometric single crystals of pyrite with euhedral shapes similar to the subunits of well crystallized framboids, biogenic starting material produced micrometric spherulitic clusters of pyrite resembling the so-called pseudo-framboids. Although further experiments are required to ensure that it can be used as biosignatures, such specific morphologies, likely related to the presence of organic matter, may help recognizing biogenic pyrite in the geological record

Fe biomineralization mirrors individual metabolic activity in a nitrate-dependent Fe(II)-oxidizer

International audienceMicrobial biomineralization sometimes leads to periplasmic encrustation, which is predicted to enhance microorganism preservation in the fossil record. Mineral precipitation within the periplasm is, however, thought to induce death, as a result of permeability loss preventing nutrient and waste transit across the cell wall. This hypothesis had, however, never been investigated down to the single cell level. Here, we cultured the nitrate reducing Fe(II) oxidizing bacteria Acidovorax sp. strain BoFeN1 that have been previously shown to promote the precipitation of a diversity of Fe minerals (lepidocrocite, goethite, Fe phosphate) encrusting the periplasm. We investigated the connection of Fe biomineralization with carbon assimilation at the single cell level, using a combination of electron microscopy and Nano-Secondary Ion Mass Spectrometry. Our analyses revealed strong individual heterogeneities of Fe biomineralization. Noteworthy, a small proportion of cells remaining free of any precipitate persisted even at advanced stages of biomineralization. Using pulse chase experiments with 13 C-acetate, we provide evidence of individual phenotypic heterogeneities of carbon assimilation, correlated with the level of Fe biomineralization. Whereas non-and moderately encrusted cells were able to assimilate acetate, higher levels of periplasmic encrustation prevented any carbon incorporation. Carbon assimilation only depended on the level of Fe encrustation and not on the nature of Fe minerals precipitated in the cell wall. Carbon assimilation decreased exponentially with increasing cell-associated Fe content. Persistence of a small proportion of non-mineralized and metabolically active cells might constitute a survival strategy in highly ferruginous environments. Eventually, our results suggest that periplasmic Fe biomineralization may provide a signature of individual metabolic status, which could be looked for in the fossil record and in modern environmental samples

Iron mineralogy across the oxycline of a lignite mine lake

International audienceIron-rich pelagic aggregates of microbial origin named “iron snow” are formed in the water column of some acidic lignite mine lakes. We investigated the evolution of Fe mineralogy across the oxycline of the Lusatian lake 77, Germany at two sampling sites differing by their pH and mixing profiles. The central basin (CB) of this lake shows a dimictic water regime with a non-permanent anoxic deep layer and a homogeneous acidic pH all over the water column (pH 3). In contrast, the northern basin (NB) is meromictic with a permanently anoxic bottom layer and a pH increase from pH 3 in the mixolimnion (superficial part of the lake) to pH 5.5 in the monimolimnion (anoxic bottom layer). Fe minerals above and below the oxycline were identified using X-ray Absorption Spectroscopy (XAS) at the Fe K-edge and further characterized down to the atomic scale by High Resolution Transmission Electron Microscopy (HRTEM) and Scanning Transmission Electron Microscopy (STEM) coupled to Energy Dispersive X-ray Spectroscopy (EDXS). We explored local Fe redox state and C speciation using Scanning Transmission X-ray Microscopy (STXM) at the Fe L2,3-edges and C K-edge. Schwertmannite [Fe8O8(OH)8-2x(SO4)x] identified as the sole Fe mineral in CB, was polycrystalline, consisting in the aggregation of nanodomains of 2–3 nm each one exhibiting the crystal structure of schwertmannite. In contrast, schwertmannite was partly (40%) converted to aluminous ferrihydrite when reaching the oxycline in NB. This mineralogical transformation was most probably due to a combination of abiotic and microbial anaerobic processes promoting pH increase and release of Fe(II) (e.g. via heterotrophic Fe(III) reduction) that induce the catalytic hydrolysis of schwertmannite to ferrihydrite. Mineral products were stabilized in the monimolimnion by the adsorption of aluminum, silicate and organic matter. Noteworthy, local Fe redox state heterogeneities were observed, with a few areas enriched in Fe(II) as evidenced by STXM analyses at the Fe L2,3-edges. These local redox heterogeneities could arise from microbial activity (e.g. Fe(III) and/or sulfate reduction). All these results provide an in-depth mineralogical overview of iron phases forming in lake 77 as a basis for future investigations of microbial vs. abiotic parameters controlling their stability and transformation

Mechanisms of Pyrite Formation Promoted by Sulfate-Reducing Bacteria in Pure Culture

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Microbial diversity involved in iron and cryptic sulfur cycling in the ferruginous, low-sulfate waters of Lake Pavin

International audienceBoth iron-and sulfur-reducing bacteria strongly impact the mineralogy of iron, but their activity has long been thought to be spatially and temporally segregated based on the higher thermodynamic yields of iron over sulfate reduction. However, recent evidence suggests that sulfur cycling can predominate even under ferruginous conditions. In this study, we investigated the potential for bacterial iron and sulfur metabolisms in the iron-rich (1.2 mM dissolved Fe 2+), sulfate-poor (< 20 μM) Lake Pavin which is expected to host large populations of iron-reducing and iron-oxidizing microorganisms influencing the mineralogy of iron precipitates in its permanently anoxic bottom waters and sediments. 16S rRNA gene ampli-con libraries from at and below the oxycline revealed that highly diverse populations of sul-fur/sulfate-reducing (SRB) and sulfur/sulfide-oxidizing bacteria represented up to 10% and 5% of the total recovered sequences in situ, respectively, which together was roughly equivalent to the fraction of putative iron cycling bacteria. In enrichment cultures amended with key iron phases identified in situ (ferric iron phosphate, ferrihydrite) or with soluble iron (Fe 2+), SRB were the most competitive microorganisms, both in the presence and absence of added sulfate. The large fraction of Sulfurospirillum, which are known to reduce thiosul-fate and sulfur but not sulfate, present in all cultures was likely supported by Fe(III)-driven sulfide oxidation. These results support the hypothesis that an active cryptic sulfur cycle interacts with iron cycling in the lake. Analyses of mineral phases showed that ferric phosphate in cultures dominated by SRB was transformed to vivianite with concomitant precipitation of iron sulfides. As colloidal FeS and vivianite have been reported in the monimo-limnion, we suggest that SRB along with iron-reducing bacteria strongly influence iron mineralogy in the water column and sediments of Lake Pavin

Microbially Induced Mineralization of Layered Mn Oxides Electroactive in Li Batteries

International audienceNanoparticles produced by bacteria, fungi, or plants generally have physicochemical properties such as size, shape, crystalline structure, magnetic properties, and stability which are difficult to obtain by chemical synthesis. For instance, Mn(II)-oxidizing organisms promote the biomineralization of manganese oxides with specific textures under ambient conditions. Controlling their crystallinity and texture may offer environmentally relevant routes of Mn oxide synthesis with potential technological applications, e.g., for energy storage. However, whereas the electrochemical activity of synthetic (abiotic) Mn oxides has been extensively studied, the electroactivity of Mn biominerals has been seldom investigated yet. Here we evaluated the electroactivity of biologically induced biominerals produced by the Mn(II)-oxidizer bacteria Pseudomonas putida strain MnB1. For this purpose, we explored the mechanisms of Mn biomineralization, including the kinetics of Mn(II) oxidation, under different conditions. Manganese speciation, biomineral structure, and texture as well as organic matter content were determined by a combination of X-ray diffraction, electron and X-ray microscopies, and thermogravimetric analyses coupled to mass spectrometry. Our results evidence the formation of an organic-inorganic composite material and a competition between the enzymatic (biotic) oxidation of Mn(II) to Mn(IV) yielding MnO2 birnessite and the abiotic formation of Mn(III), of which the ratio depends on oxygenation levels and activity of the bacteria. We reveal that a subtle control over the conditions of the microbial environment orients the birnessite to Mn(III)-phases ratio and the porosity of the assembly, which both strongly impact the bulk electroactivity of the composite biomineral. The electrochemical properties were tested in lithium battery configuration and exhibit very appealing performances (voltage, capacity, reversibility, and power capability), thanks to the specific texture resulting from the microbially driven synthesis route. Given that such electroactive Mn biominerals are widespread in the environment, our study opens an alternative route for the synthesis of performing electrode materials under environment-friendly conditions

Significance, mechanisms and environmental implications of microbial biomineralization

International audienceMicroorganisms can mediate the formation of minerals by a process called biomineralization. This process offers an efficient way to sequester inorganic pollutants within relatively stable solid phases. Here we review some of the main mechanisms involved in the mediation of mineral precipitation by microorganisms. This includes supersaturation caused by metabolic activity, the triggering of nucleation by production of more or less specific organic molecules, and the impact of mineral growth. While these processes have been widely studied in the laboratory, assessment of their importance in the environment is more difficult. Weillustrate this difficulty using a case study on an As-contaminated acid mine drainage located in the South of France (Carnoule' s, Gard). In particular, we explore the potential relationships that might exist between microbial diversity and mineral precipitation. The present review, far from being exhaustive, highlights some recent advances in the field of biomineralogy and provides non-specialists an introduction to some of the main approaches and some questions that remain unanswered

Calcification and Diagenesis of Bacterial Colonies

Evidencing ancient interspecific associations in the fossil record may be challenging, particularly when bacterial organisms have most likely been degraded during diagenesis. Yet, documenting ancient interspecific associations may provide valuable insights into paleoenvironmental conditions and paleocommunities. Here, we report the multiscale characterization of contemporary and fossilized calcifying bacterial colonies found on contemporary shrimps from Mexico (La Paz Bay) and on 160-Ma old fossilized decapods (shrimps) from the Lagerstätte of La Voulte-sur-Rhône (France), respectively. We document the fine scale morphology, the inorganic composition and the organic signatures of both the contemporary and fossilized structures formed by these bacterial colonies using a combination of electron microscopies and synchrotron-based scanning transmission X-ray microscopy. In addition to discussing the mechanisms of carbonate precipitation by such bacterial colonies, the present study illustrates the degradation of bacterial remains occurring during diagenesis