Biogenic precipitation of manganese oxides and enrichment of heavy metals at acidic soil pH

Abstract

Natural Mn oxides are largely biogenic in origin, formed via the microbial oxidation of Mn(II). These minerals are extremely efficient scavengers of heavy metals, yet to date microbial Mn oxide precipitation and subsequent heavy metal sorption have received little attention in mining-impacted environments, where heavy metal concentrations are elevated but (bio)geochemical conditions are typically unfavourable for both abiotic and biogenic Mn oxide precipitation, featuring acidic pH and low organic carbon contents. Here we investigate the formation of Mn oxide (bio)geochemical barrier layers, and the immobilisation of heavy metals in these layers, in soil profiles from a former uranium mining site in Ronneburg, Germany. Detailed soil profiling shows the site has an acidic soil pH that varies from 4.7 to 5.1 and Eh values from 640 to 660mV. Using synchrotron X-ray diffraction and X-ray absorption spectroscopy, together with scanning electron microscopy and electron microprobe analysis, we find that the dominant Mn oxide present in the Mn oxide layers is a poorly crystalline hexagonal birnessite, akin to synthetic δ-MnO2, covering and cementing quartz grains. Using phylogenetic analysis based on 16S rDNA, we identify and characterise six strains of manganese oxidising bacteria (MOB) from the acidic Mn oxide layers which we subsequently culture to produce poorly crystalline hexagonal birnessite akin to that found at the study site. Specifically, we identify three Gram-positive spore-forming firmicutes affiliated to Bacillus safensis, Bacillus altitudinis and Brevibacillus reuszeri, which are able to oxidise Mn after initiating spore formation, two Gram-positive actinobacteria belonging to the genera Arthrobacter and Frondihabitans, and one Gram-negative proteobacteria belonging to the genus Sphingomonas. Geochemical thermodynamic speciation modelling indicates that the abiotic precipitation of Mn oxides in the Mn oxide layers is unfavourable and we suggest that the Mn oxides in the (bio)geochemical barriers at our study site are biogenically precipitated in an acidic soil environment. To our knowledge, this is the first report to identify the above six bacterial strains, and specifically identify spore-forming bacteria, as MOB in an acidic soil environment. We find that the poorly crystalline hexagonal birnessite precipitated in the Mn oxide layers efficiently immobilises Ba, Ni, Co, Cd, Zn and Ce, and as such we find that MOB and biogenically precipitated Mn oxides can exert a strong control on the fate and mobility of metals in mining-impacted environments.