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Geomicrobiology Journal | Sjöberg Et Geomicrobiology Journal ISSN: 0149-0451 (Print) 1521-0529 (Online) Journal homepage: http://www.tandfonline.com/loi/ugmb20 Microbial Communities Inhabiting a Rare Earth Element Enriched Birnessite-Type Manganese Deposit in the Ytterby Mine, Sweden Susanne Sjöberg, Nolwenn Callac, Bert Allard, Rienk H. Smittenberg & Christophe Dupraz To cite this article: Susanne Sjöberg, Nolwenn Callac, Bert Allard, Rienk H. Smittenberg & Christophe Dupraz (2018): Microbial Communities Inhabiting a Rare Earth Element Enriched Birnessite-Type Manganese Deposit in the Ytterby Mine, Sweden, Geomicrobiology Journal, DOI: 10.1080/01490451.2018.1444690 To link to this article: https://doi.org/10.1080/01490451.2018.1444690 © 2018 The Author(s). Published by Informa UK Limited, trading as Taylor & Francis Group, followed by the correct licence statement Published online: 03 Apr 2018. Submit your article to this journal View related articles View Crossmark data Full Terms & Conditions of access and use can be found at http://www.tandfonline.com/action/journalInformation?journalCode=ugmb20 GEOMICROBIOLOGY JOURNAL, 2018 https://doi.org/10.1080/01490451.2018.1444690 Microbial Communities Inhabiting a Rare Earth Element Enriched Birnessite-Type Manganese Deposit in the Ytterby Mine, Sweden Susanne Sjoberg€ a, Nolwenn Callaca,c, Bert Allardb, Rienk H. Smittenberga and Christophe Dupraza aDepartment of Geological Sciences, Stockholm University, SE Stockholm, Sweden; bMan-Technology-Environment Research Centre (MTM), Orebro€ University, SE Orebro,€ Sweden; cDepartment of Paleobiology, Swedish Museum of Natural History, Stockholm, Sweden ABSTRACT ARTICLE HISTORY The dominant initial phase formed during microbially mediated manganese oxidation is a poorly Received 16 December 2017 crystalline birnessite-type phyllomanganate. The occurrence of manganese deposits containing this Accepted 20 February 2018 mineral is of interest for increased understanding of microbial involvement in the manganese cycle. A KEYWORDS fi culture independent molecular approach is used as a rst step to investigate the role of microorganisms in Birnessite; microbial forming rare earth element enriched birnessite-type manganese oxides, associated with water bearing diversity; manganese rock fractures in a tunnel of the Ytterby mine, Sweden. 16S rRNA gene results show that the chemotrophic oxidizing bacteria; bacterial communities are diverse and include a high percentage of uncultured unclassified bacteria while organomineralization; archaeal diversity is low with Thaumarchaeota almost exclusively dominating the population. Ytterby subsurface microbiology clones are frequently most similar to clones isolated from subsurface environments, low temperature milieus and/or settings rich in metals. Overall, bacteria are dominant compared to archaea. Both bacterial and archaeal abundances are up to four orders of magnitude higher in manganese samples than in fracture water. Potential players in the manganese cycling are mainly found within the ferromanganese genera Hyphomicrobium and Pedomicrobium, and a group of Bacteroidetes sequences that cluster within an uncultured novel genus most closely related to the Terrimonas. This study strongly suggest that the production of the YBS deposit is microbially mediated. Introduction deposits (Carmichael et al. 2013; Carmichael and Br€auer 2015, Microbially mediated and abiotic processes involved in manga- and references therein; Northup et al. 2003; Saiz-Jimenez et al. nese (Mn) cycling strongly interact at the biosphere-lithosphere 2012;Santellietal.2010;Spildeetal.2005). interface, allowing the investigation of cryptic cross-linkages The Ytterby mine, once a quartz and feldspar mine, known within the biogeochemical cycles (e.g., Hansel et al. 2015). Oxi- for the discovery of scandium, yttrium, tantalum and five of the dation of reduced species of iron (Fe) and Mn may result in the rare earth elements (REE), was recently found to host a REE+Y precipitation and accumulation of brown to black insoluble enriched Mn deposit denoted YBS, Ytterby black substance oxides, often associated with seepages of reduced water into (Sjoberg€ et al. 2017). Elemental analysis and phase analysis by aerobic environments such as water-bearing rock fractures that XRD indicate that the dominant phase is a birnessite-type Mn crop out in caves or tunnels (Frierdich et al. 2011; Nealson oxide with low Fe content but with traces of organics. Poorly 2006; Pedersen 1997). This solid-liquid and oxic-anoxic inter- crystalline birnessite-like phyllomanganates often represent the face provides favorable conditions for biofilm development and initial phase precipitated by bacteria and fungi during micro- strong microbe-mineral interactions (Donlan 2002; Pedersen bially mediated Mn oxidation (Hansel and Learman 2016). 1997). Although thermodynamically favorable under oxic con- Electron paramagnetic resonance (EPR) spectroscopy indicates ditions (Ehrlich 1978; Stumm and Morgan 1981), oxidation of a microbial origin of a large fraction of the manganese oxide Mn is a slow process, which can take years to complete in envi- precipitates (Sjoberg€ et al. 2017). ronments at circumneutral pH (Krauskopf 1957;Teboetal. The Mn precipitates in the Ytterby mine provide a window 2004). The catalytic role that microbial communities and pro- into the complex Mn cycle and on the development of micro- cesses have in the Mn redox cycle is well documented (Hansel bial communities in special conditions, such as low constant and Learman 2016). Nevertheless, the microbial mechanisms temperature (8C), absence of light, low nutrient and carbon that are driving these processes remain to some extent unknown, sources, and high metal content. Here a culture independent but Mn oxidation involves direct (enzymatic) or indirect antioxi- molecular phylogenetic approach is used to characterize this dative (interactive with Reactive Oxygen Species (ROS)) pro- newly observed underground ecosystem. The objectives are to cesses and possibly also lithotrophy (Hansel and Learman 2016; provide further insight into the putative biogenic origin of the Nealson 2006;Teboetal.2004). Only a few molecular 16S rRNA YBS and to identify and characterize any associated microbial phylogenetic studies have been conducted on Mn cave or tunnel community. CONTACT Susanne Sjoberg€ [email protected] Department of Geological Sciences, Stockholm University, SE-106 91 Stockholm, Sweden. © 2018 The Author(s). Published by Informa UK Limited, trading as Taylor & Francis Group, followed by the correct licence statement This is an Open Access article distributed under the terms of the Creative Commons Attribution-NonCommercial-NoDerivatives License (http://creativecommons.org/licenses/by-nc-nd/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited, and is not altered, transformed, or built upon in any way. 2 S. SJOBERG€ ET AL. Materials and methods carbon and silicon) was 82% Mn, 13.5% Ca and 2§0.5% REE +Y, with all other metals being less than 2% in total (Sjoberg€ Study site and geochemical data on the Ytterby black et al. 2017). The dominant mineral phase was a birnessite-type substance (YBS) phyllomanganate, as evidenced by XRD, with minor fractions The Ytterby mine is located on Resaro,€ about 25 km NE of of quartz, plagioclase and calcium carbonate (likely arising Stockholm, Sweden (Figure 1). The Mn accumulations (YBS) from the underlying bedrock and underlying mineralized cal- are associated with water-bearing rock fractures in a subterra- cium carbonate precipitate). nean tunnel leading to the main shaft of the mine (Figure 1). Characterization of the YBS by IR- and EPR-spectroscopy, The tunnel is located at shallow depth, 29 m below ground sur- analysis of concentrations and isotopic signatures of carbon face and 5 m above the Baltic Sea mean sea level, and was built and nitrogen, sequential extraction procedures and lipid analy- to convert the former mine into a fuel deposit for the Swedish sis indicated the presence of about 1.8% carbon, one third of Armed Forces. The 400 m long tunnel links the old mine shaft which was organic (Sjoberg€ et al, 2017). In a previous study by with a quay located to the NE of the quarry along the Baltic Sea Sjoberg€ et al. (2017), a microbial origin of a major fraction of coastline. In this stretch the tunnel passes through granitic and the manganese oxide precipitation was suggested by the EPR- mafic rocks of varying chemical composition and metamorphic spectroscopy: none of the metals appeared to be present as grade. The YBS occur as rock wall deposits in association with metal-organic or humic bound species. The organic matter was – a2 3 mm thick underlying blanket of mineralized calcium car- predominantly hopanoids, and the presence of C31 to C35 bonate precipitate (Figure 1). extended side chain species was a distinct indication of bacterial The YBS deposit is located in the unsaturated zone of the presence. Environmental scanning electron microscopy tunnel section where water bearing fractures provide a continu- (ESEM-EDS) confirmed the elemental analysis and showed ous supply of water to the fully oxidized tunnel environment three dominant microstructures in the YBS: (1) Dendritic/ which holds a nearly constant temperature of 8C year round. shrub-like, (2) microspherolitic/botryoidal, and (3) filaments of Artificial lighting is used for purposes of mine maintenance, in various thicknesses. Cross-sections of the dendritic
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