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Licentiate thesis Geochemistry Microbially mediated formation of birnessite-type manganese oxides and subsequent incorporation of rare earth elements, Ytterby mine, Sweden Susanne Sjöberg Stockholm 2017 Department of Geological Sciences Stockholm University SE-106 91 Stockholm Abstract Microbes exert extensive control on redox element cycles. They participate directly or indirectly in the concentration and fractionation of elements by influencing the partitioning between soluble and insoluble species. Putative microbially mediated manganese (Mn) oxides of the birnessite-type, enriched in rare earth elements (REE) + yttrium (Y) were recently found in the Ytterby mine, Sweden. A poorly crystalline birnessite-type phyllomanganate is regarded as the predominant initial phase formed during microbial Mn oxidation. Owing to a higher specific surface area, this biomineral also enhances the known sorption property of Mn oxides with respect to heavy metals (e.g. REE) and therefore has considerable environmental impact. The concentration of REE + Y (2±0.5% of total mass, excluding oxygen, carbon and silicon) in the Ytterby Mn oxide deposit is among the highest ever observed in secondary precipitates with Mn and/or iron. Sequential extraction provides evidence of a mineral structure where the REE+Y are firmly included, even at pH as low as 1.5. Concentration ratios of Mn oxide precipitates to fracture water indicate a strong preference for the trivalent REE+Y over divalent and monovalent metals. A culture independent molecular phylogenetic approach was adopted as a first step to analyze the processes that microbes mediate in this environment and specifically how the microbial communities interact with the Mn oxides. Plausible players in the formation of the investigated birnessite-type Mn oxides are mainly found within the ferromanganese genera Hyphomicrobium and Pedomicrobium and a newly identified Ytterby Bacteroidetes cluster most closely related to the Terrimonas. Data also indicate that the detected microorganisms are related to the environmental constraints of the site including low constant temperature (8°C), absence of light, high metal content and possibly proximity to the former storage of petroleum products. Keywords: microbial diversity, manganese oxides, birnessite, rare earth elements, subterranean, Ytterby mine Sammanfattning Elementcykler kan drivas av redoxprocesser, vilka sker spontant på Jordens yta så länge de är termodynamiskt fördelaktiga. Mikroorganismer kan påverka och dra nytta av dessa processer så länge den mikrobiella aktiviteten är mer effektiv än den inorganiska processen. Under dessa medlingsprocesser påverkar mikroberna fördelningen mellan lösliga species och olösliga species och vice versa. Genom denna inblandning i produktion och/eller nedbrytning av mineral, har mikroberna stort inflytande över elementcykler och bidrar därmed direkt eller indirekt till koncentration och fraktionering av specifika element. I Ytterby gruva (Sverige) upptäcktes nyligen en ackumulation av en förmodat mikrobiellt bildad variant av manganoxiden birnessit, anrikad med avseende på sällsynta jordartsmetaller (REE) och yttrium (Y). En lågristallin variant av birnessit är den dominerande intiala fasen som produceras vid mikrobiellt bildad manganoxid. Tack vare en större specifik yta har denna mikrobiellt bildade fas egenskaper som ger en förhöjd sorptionskapacitet med avseende på tungmetaller i jämförelse med andra Mn-oxider (som generellt också har mycket hög sorptionskapacitet). Dessa mikrob-medierade Mn-oxider har därför avsevärd påverkan på miljön. Ytterby-birnessiten innehåller 2±0.5 vikt-% REE+Y (exklusive syre, kol och kisel). Detta är bland de högsta REE+Y-halter som observerats i sekundära utfällningar innehållande REE. Sekventiell lakning av Ytterby-birnessiten antyder en mineralstruktur där REE+Y är fast inkorporerade, även vid pH så lågt som 1.5. Koncentrationsförhållandet mellan de utfällda manganoxiderna och sprickvattnet tyder på en stark preferens för de trivalenta REE+Y över divalenta och monovalenta metaller. Molekylär fylogenetisk analys användes som ett första steg för att förstå processerna som mikrober medlar i denna miljö, och specifikt hur de mikrobiella samhällena interagerar med Mn-oxiderna. Troliga medlare i bildandet av de undersökta Mn-oxiderna av birnessit-typ finns främst bland ferromangansläktena Hyphomicrobium och Pedomicrobium (P. Manganicum) och ett nyupptäckt Bacteroidetes kluster som är närmast släkt med Terrimonas. Data tyder också på att de identifierade mikroorganismerna är relaterade till de faktorer som definierar ackumulationsmiljön: låg konstant temperatur (8°C), avsaknad av ljus, högt metallinnehåll och möjligen också närheten till den tidigare lagringen av petroleumprodukter. Nyckelord: mikrobiell diversitet, manganoxider, birnessit, sällsynta jordartsmetaller, underjordisk, Ytterby mine List of papers This thesis is based on the following papers which are referred to in the text by their Roman numerals. I. Sjöberg S, Allard B, Rattray JE, Callac N, Grawunder A, Ivarsson M, Sjöberg V, Karlsson S, Skelton A and Dupraz C. (2017). Rare earth element enriched birnessite in water-bearing fractures, the Ytterby mine, Sweden. Appl Geochem 78:158-171. II. Sjöberg S, Callac N, Allard B, Smittenberg R and Dupraz C. (2017). Microbial communities inhabiting a birnessite-type manganese deposit, the Ytterby mine, Sweden. (submitted). Table of contents 1. Introduction 2. Microbially mediated Mn oxides – formation and trace metal accumulation 2.1 Microbial communities, organic matter and mineral precipitation 2.2 Microbially mediated Mn oxides 2.3 Accumulation of metals by Mn oxides 3. Materials and methods 3.1 Background 3.2 Sampling and characterization of the birnessite-type Mn oxide (paper I) 3.3 Microbial communities inhabiting the birnessite-type Mn oxides (paper II) 4. Results and discussion 4.1 Composition of the birnessite-type Mn oxide (paper I) 4.2 Indicators of microbial involvement in the production of the birnessite-type Mn oxide (paper I) 4.3 Microbial communities inhabiting the YBS (paper II) 4.4 Potential mechanisms for the formation of the birnessite-type Mn oxides (paper II) 4.5 Redistribution of REE and enrichment in the birnessite-type Mn oxide in the Ytterby mine (paper I) 4.6 A metal stressed microbial community? 5. Conclusions 6. Future research areas Acknowledgments References Appendix A. paper 1 Appendix B. paper 2 1. Introduction Element cycles can be driven by redox processes, which can spontaneously take place inorganically at the surface of the Earth. Microbes are able to influence these processes and derive advantages from them, provided that their activity is more efficient than the inorganic process (Krauskopf 1957; Pedersen 2005). In these mediations microbes alter the litho- and hydrosphere by transforming soluble species into insoluble precipitates and vice versa (Pedersen 2005). While being involved in production and/or dissolution of minerals, microbes exert extensive control on the cycling of elements and participate, directly or indirectly, in concentration and fractionation of specific elements. The manganese (Mn) biogeochemical cycle involves cross-linkages between microbial and abiotic processes and multiple element cycles (Hansel et al. 2015). The interaction between Mn and microorganisms in the oxidative Mn cycle may result in the formation of Mn oxides, commonly in the form of poorly crystalline birnessite-type phyllomanganates with hexagonal symmetry (Villalobos et al. 2003; Tebo et al. 2004; Bargar et al. 2005; Villalobos et al. 2006; Santelli et al. 2011; Hansel and Learman 2016). The catalytic function that microbial communities and processes have in the Mn redox cycle is well documented (Hansel and Learman 2016). Nevertheless, the microbial mechanisms driving these processes, and the properties of the mineral product, remain to some extent unknown. The former quartz and feldspar mine in Ytterby is the type location for scandium, yttrium, tantalum and five of the rare earth elements (REE). Recent investigations have revealed that the mine hosts a black REE+Y enriched Mn deposit, hereafter referred to as the Ytterby black substance (YBS) (Sjöberg 2014). Phase analysis by X-ray diffraction (XRD) and elemental analysis show that the dominating phase is a birnessite-type Mn oxide with traces of organics and low Fe content (Sjöberg 2014). Electron paramagnetic resonance (EPR)-spectroscopy and lipid biomarker analyses indicate that the formation of the Mn deposit is induced by a microbial community (Sjöberg 2014). This site provides a window on the complex interaction between microbes and Mn minerals and the subsequent accumulation of trace elements. Objectives This thesis aims to increase the understanding of mechanisms involved in the formation and accumulation of the putative microbially mediated REE+Y enriched birnessite-type Mn oxides. Two main questions guide the approaches used in this work: Q1: How are the REE+Y associated with the birnessite-type Mn oxides? Q2: What microbial communities inhabit the Mn deposit and is it possible within these populations to identify Mn oxidizers and investigate their role in the formation of the birnessite-type Mn oxides? Preliminary results on composition, structure and origin of the YBS as reported in Sjöberg (2014), are confirmed by repeated elemental, phase, spectroscopic and organic fraction analyses. A sequential extraction procedure is conducted to provide information on the nature of the REE association
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  • Supporting Information

    Supporting Information

    Supporting Information Brown et al. 10.1073/pnas.1114476109 SI Materials and Methods and silver enhancement was not required. Electron microscopy Strains and Conditions. A. tumefaciens C58 was grown in Luria– was performed on a JEOL JEM1010 at 60 kV, equipped with a Bertani (LB) broth medium or in AT minimal medium (1) TemCam-F416 (TVIPS) digital camera. supplemented with 0.5% (wt/vol) glucose and 15 mM ammo- nium sulfate and 0.1 mM acetosyringone at 26 °C. S. meliloti Electron Microscopy. Droplets of exponentially growing cultures fi 1021 was grown in LB medium supplemented with 2.5 mM were deposited onto a piece of para lm and E.M. carbon-for- fl CaCl and 2.5 mM MgSO at 26 °C. Brucella abortus 544 was mvar-coated copper grids (200 mesh) were oated onto the 2 4 droplets for 2 min. Excess liquid was removed with filter paper, grown in 2YT liquid medium at 37 °C and O. anthropi LMG 3331 fl was grown in LB medium at 30 °C. H. denitrificans was grown in and the grids were quickly washed four times oating onto Hyphomicrobium medium 337 containing 0.4% methylamine droplets of double distilled water, transferred to droplets of 1% hydrochloride (2) at 26 °C without shaking. P. hirschii was grown uranyl acetate in water for 2 min, washed once in double distilled on MMB medium (3) at 26 °C. When necessary, kanamycin was water, dried, and subjected to electron microscopy as described above for D-cys labeling. used at 100 μg/mL and 1 mM isopropyl-α-D-thio-galactoside (IPTG) was used as an inducer.