Metagenomes from microbial populations beneath a chromium waste tip give insight into the mechanism of Cr (VI) reduction

Douglas I Stewart; Elton J R Vasconcelos; Ian T Burke; Alison Baker

doi:10.1016/j.scitotenv.2024.172507

Metagenomes from microbial populations beneath a chromium waste tip give insight into the mechanism of Cr (VI) reduction

Sci Total Environ. 2024 Apr 23:931:172507. doi: 10.1016/j.scitotenv.2024.172507. Online ahead of print.

Authors

Douglas I Stewart¹, Elton J R Vasconcelos², Ian T Burke³, Alison Baker⁴

Affiliations

¹ School of Civil Engineering, University of Leeds, Leeds LS2 9JT, UK. Electronic address: d.i.stewart@leeds.ac.uk.
² Leeds Omics, University of Leeds, Leeds LS2 9JT, UK. Electronic address: E.Vasconcelos@leeds.ac.uk.
³ School of Earth and Environment, University of Leeds, Leeds LS2 9JT, UK. Electronic address: i.t.burke@leeds.ac.uk.
⁴ School of Molecular and Cellular Biology, University of Leeds, Leeds LS2 9JT, UK. Electronic address: a.baker@leeds.ac.uk.

PMID: 38657818
DOI: 10.1016/j.scitotenv.2024.172507

Abstract

Dumped Chromium Ore Processing Residue (COPR) at legacy sites poses a threat to health through leaching of toxic Cr(VI) into groundwater. Previous work implicates microbial activity in reducing Cr(VI) to less mobile and toxic Cr(III), but the mechanism has not been explored. To address this question a combined metagenomic and geochemical study was undertaken. Soil samples from below the COPR waste were used to establish anaerobic microcosms which were challenged with Cr(VI), with or without acetate as an electron donor, and incubated for 70 days. Cr was rapidly reduced in both systems, which also reduced nitrate, nitrite then sulfate, but this sequence was accelerated in the acetate amended microcosms. 16S rRNA gene sequencing revealed that the original soil sample was diverse but both microcosm systems became less diverse by the end of the experiment. A high proportion of 16S rRNA gene reads and metagenome-assembled genomes (MAGs) with high completeness could not be taxonomically classified, highlighting the distinctiveness of these alkaline Cr impacted systems. Examination of the coding capacity revealed widespread capability for metal tolerance and Fe uptake and storage, and both populations possessed metabolic capability to degrade a wide range of organic molecules. The relative abundance of genes for fatty acid degradation was 4× higher in the unamended compared to the acetate amended system, whereas the capacity for dissimilatory sulfate metabolism was 3× higher in the acetate amended system. We demonstrate that naturally occurring in situ bacterial populations have the metabolic capability to couple acetate oxidation to sequential reduction of electron acceptors which can reduce Cr(VI) to less mobile and toxic Cr(III), and that microbially produced sulfide may be important in reductive precipitation of chromate. This capability could be harnessed to create a Cr(VI) trap-zone beneath COPR tips without the need to disturb the waste.

Keywords: Acetate; Alkaline environment; Anaerobic sulfite reduction; COPR; Dissimilatory sulfate reduction; Whole genome sequencing.