Microbiomes in a manganese oxide producing ecosystem in the Ytterby mine, Sweden: impact on metal mobility

Abstract

Microbe-mediated precipitation of Mn-oxides enriched in rare earth elements (REE) and other trace elements was discovered in tunnels leading to the main shaft of the Ytterby mine, Sweden. Defining the spatial distribution of microorganisms and elements in this ecosystem provide a better understanding of specific niches and parameters driving the emergence of these communities and associated mineral precipitates. Along with elemental analyses, high-throughput sequencing of the following four subsystems were conducted: (1) water seeping from a rock fracture into the tunnel, (2) Mn-oxides and associated biofilm; referred to as the Ytterby Black Substance (YBS) biofilm (3) biofilm forming bubbles on the Mn-oxides; referred to as the bubble biofilm, and (4) fracture water that has passed through the biofilms. Each subsystem hosts a specific collection of microorganisms. Differentially abundant bacteria in the YBS biofilm were identified within the Rhizobiales (e.g. Pedomicrobium), PLTA13 Gammaproteobacteria, Pirellulaceae, Hyphomonadaceae, Blastocatellia and Nitrospira. These taxa, likely driving the Mn-oxide production, were not detected in the fracture water. This biofilm binds Mn, REE and other trace elements in an efficient, dynamic process, as indicated by substantial depletion of these metals from the fracture water as it passes through the Mn deposit zone. Microbe-mediated oxidation of Mn(II) and formation of Mn(III/IV)-oxides can thus have considerable local environmental impact by removing metals from aquatic environments.

Microbe-Mediated Mn Oxidation—A Proposed Model of Mineral Formation

“…Members of the Pedobacter and Nevskia genera were previously not known to oxidize Mn while the three other taxa were known to. Members of the Nevskia genus were previously shown to be highly abundant at the field site, while the relative abundance of the other strains only accounted for a maximum of 0.09% [8,32]. Hydrogenophaga spp.…”

“…The vast majority of observed water bearing fractures are associated with Mn precipitates overlying a lithified layer of CaCO 3 , while only a few are associated with moonmilk deposits, a soft, not lithified rock wall coating of CaCO 3 [14]. The main components of the bulk precipitate are Mn (500 g/kg), Ca (65 g/kg), and REE (10 g/kg), and the predominant mineral is a microbe-mediated birnessite-type Mn oxide [8,15]. Powder X-ray diffractometry indicates that other poorly crystalline Mn phases are also present [15].…”

“…CaCO3 [14]. The main components of the bulk precipitate are Mn (500 g/kg), Ca (65 g/kg), and REE (10 g/kg), and the predominant mineral is a microbe-mediated birnessite-type Mn oxide [8,15]. Powder X-ray diffractometry indicates that other poorly crystalline Mn phases are also present [15].…”

“…cells. Nevskia spp., which are epineuston stalked bacteria (bacteria living at the water surface and producing thin extensions out of the cell wall), representing the most abundant genus in a micrometer thick gas-trapping biofilm located on the surface of the precipitated Mn oxides in Ytterby (see details in [8,32]). Its involvement in the Mn oxide producing ecosystem is not yet clear, but results from this study indicate that Nevskia spp.…”

“…The precipitates occur as rock wall coatings associated with water-bearing fractures that emerge into a fully oxidized tunnel environment. In a recent study, the microbiomes in this ecosystem and their impact on metal mobility, were defined [8]. The study found that the fracture water was substantially depleted in Mn and other trace elements as it passes through the Mn precipitation zone down the approximately 2 m tall rock wall, and that a specific assemblage of bacteria are driving Mn oxidation and precipitation, thus indicating that these microbial groups have critical control on the end product (i.e., Mn oxides).…”