Dataset Information

Biotransformation of Scheelite CaWO₄ by the Extreme Thermoacidophile Metallosphaera sedula: Tungsten-Microbial Interface.

ABSTRACT: The tungsten-microbial interactions and microbial bioprocessing of tungsten ores, which are still underexplored, are the focus of the current study. Here we show that the biotransformation of tungsten mineral scheelite performed by the extreme thermoacidophile Metallosphaera sedula leads to the breakage of scheelite structure and subsequent tungsten solubilization. Total soluble tungsten is significantly higher in cultures containing M. sedula grown on scheelite than the abiotic control, indicating active bioleaching. Advanced analytical electron microscopy was used in order to achieve nanoscale resolution ultrastructural studies of M. sedula grown on tungsten bearing scheelite. In particular, we describe that M. sedula mediated the biotransformation of scheelite, which was accompanied by the release of tungsten into solution and tungsten biomineralization of the cell surface. Furthermore, we observed intracellular incorporation of redox heterogenous Mn- and Fe-containing nano-clusters. Our results highlight unique metallophilic life in hostile environments extending the knowledge of tungsten biogeochemistry. Based on these findings biohydrometallurgical processing of tungsten ores can be further explored. Importantly, biogenic tungsten carbide-like nanolayers described herein are potential targets for developing nanomaterial biotechnology.

SUBMITTER: Blazevic A

PROVIDER: S-EPMC6614383 | biostudies-literature | 2019

REPOSITORIES: biostudies-literature

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Publications

Biotransformation of Scheelite CaWO4 by the Extreme Thermoacidophile Metallosphaera sedula: Tungsten-Microbial Interface.

Blazevic Amir A Albu Mihaela M Mitsche Stefan S Rittmann Simon K-M R SKR Habler Gerlinde G Milojevic Tetyana T

Frontiers in microbiology 20190702

The tungsten-microbial interactions and microbial bioprocessing of tungsten ores, which are still underexplored, are the focus of the current study. Here we show that the biotransformation of tungsten mineral scheelite performed by the extreme thermoacidophile Metallosphaera sedula leads to the breakage of scheelite structure and subsequent tungsten solubilization. Total soluble tungsten is significantly higher in cultures containing M. sedula grown on scheelite than the abiotic co ...[more]

PMID: 31312192

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Project description:Inorganic systems based upon polyoxometalate (POM) clusters provide an experimental approach to develop artificial life. These artificial symmetric anionic macromolecules with oxidometalate polyhedra as building blocks were shown to be well suited as inorganic frameworks for complex self-assembling and organizing systems with emergent properties. Analogously to mineral cells based on iron sulfides, POMs are considered as inorganic cells in facilitating prelife chemical processes and displaying "life-like" characteristics. However, the relevance of POMs to life-sustaining processes (e.g., microbial respiration) has not yet been addressed, while iron sulfides are very well known as ubiquitous mineral precursors and energy sources for chemolithotrophic metabolism. Metallosphaera sedula is an extreme metallophilic and thermoacidophilic archaeon, which flourishes in hot acid and respires by metal oxidation. In the present study we provide our observations on M. sedula cultivated on tungsten polyoxometalate (W-POM). The decomposition of W-POM macromolecular clusters and the appearance of low molecular weight W species (e.g., WO) in the presence of M. sedula have been detected by electrospray ionization mass spectrometry (ESI-MS) analysis. Here, we document the presence of metalloorganic assemblages at the interface between M. sedula and W-POM resolved down to the nanometer scale using scanning and transmission electron microscopy (SEM and TEM) coupled to electron energy loss spectroscopy (EELS). High-resolution TEM (HR-TEM) and selected-area electron diffraction (SAED) patterns indicated the deposition of redox heterogeneous tungsten species on the S-layer of M. sedula along with the accumulation of intracellular tungsten-bearing nanoparticles, i.e., clusters of tungsten atoms. These results reveal the effectiveness of the analytical spectroscopy coupled to the wet chemistry approach as a tool in the analysis of metal-microbial interactions and microbial cultivation on supramolecular self-assemblages based on inorganic metal clusters. We discuss the possible mechanism of W-POM decomposition by M. sedula in light of unique electrochemical properties of POMs. The findings presented herein highlight unique metallophilicity in hostile environments, extending our knowledge of the relevance of POMs to life-sustaining processes, understanding of the transition of POMs as inorganic prebiotic model to life-sustainable material precursors and revealing biogenic signatures obtained after the decomposition of an artificial inorganic compound, which previously was not associated with any living matter.

Project description:Thermomacidophilic archaea, such as Metallosphaera sedula, are lithoautotrophs that occupy metal-rich environments. In previous studies, a M. sedula mutant lacking the primary copper efflux transporter, CopA, became copper sensitive. In contrast, the basis for supra-normal copper resistance remained unclear in the spontaneous M. sedula mutant, CuR1. Here, transcriptomic analysis of copper-shocked cultures indicated that CuR1 had a unique regulatory response to metal challenge corresponding to up-regulation of 55 genes. Genome re-sequencing identified 17 confirmed mutations unique to CuR1 that were likely to change gene function. Of these, 12 mapped to genes with annotated function associated with transcription, metabolism or transport. These mutations included 7 non-synonymous substitutions, 4 insertions and 1 deletion. One of the insertion mutations mapped to pseudogene, Msed_1517, and extended its reading frame an additional 209 amino acids. The extended mutant allele was identified as a homolog of Pho4, a family of phosphate symporters that include the bacterial PitA proteins. Orthologs of this allele were apparent in related extremely thermoacidophilic species, suggesting M. sedula was naturally lacking this gene. Phosphate transport studies combined with physiologic analysis demonstrated M. sedula PitA was a low affinity high velocity secondary transporter implicated in copper resistance and arsenate sensitivity. Genetic analysis demonstrated spontaneous arsenate resistant mutants derived from CuR1 all underwent mutation in pitA and non-selectively became copper resistant. Taken together, these results point to archaeal PitA as a key requirement for the increased metal resistance of strain CuR1 and its accelerated capacity for copper bioleaching. The study comprises 5 samples, described in detail below. WT_CuR1: Differential transcriptional response of Metallosphaera sedula DSM 5348, WT, to the supra-normal copper resistant spontaneous Metallosphaera sedula mutant, CuR1 under normal growth conditions. This experiment was done to analyze the differential transcription of WT cells compared with CuR1 cells at mid log phase. WT-15_CuR1-15: Differential transcription of Metallosphaera cells under sub-inhibitory copper challenge (2.0 mM). This experiment was done to analyze the differential transcription of Metallosphaera sedula WT and CuR1 15 minutes post copper challenge. The copper cultures were harvested 15 minutes after the shock. WT-60_CuR1-60: Differential transcription of Metallosphaera cells under sub-inhibitory copper challenge (2.0 mM). This experiment was done to analyze the differential transcription of Metallosphaera sedula WT and CuR1 60 minutes post copper challenge. The copper cultures were harvested 60 minutes after the shock. WT-15_WT-60: Differential transcription of Metallosphaera cells under sub-inhibitory copper challenge (2.0 mM). This experiment was done to analyze the differential transcription of Metallosphaera sedula WT 15 and 60 minutes post copper challenge. The copper cultures were harvested 15 and 60 minutes after the shock, respectively. CuR1-15_CuR1-60: Differential transcription of Metallosphaera cells under sub-inhibitory copper challenge (2.0 mM). This experiment was done to analyze the differential transcription of Metallosphaera sedula CuR1 15 and 60 minutes post copper challenge. The copper cultures were harvested 15 and 60 minutes after the shock, respectively.

Dataset Information

Biotransformation of Scheelite CaWO₄ by the Extreme Thermoacidophile Metallosphaera sedula: Tungsten-Microbial Interface.

Publications

Biotransformation of Scheelite CaWO<sub>4</sub> by the Extreme Thermoacidophile <i>Metallosphaera sedula</i>: Tungsten-Microbial Interface.

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