Multi-omics reveal various potential antimonate reductases from phylogenetically diverse microorganisms

Abstract

While previous work has demonstrated that antimonate (Sb(V)) can be bio-reduced with methane as the sole electron donor, the microorganisms responsible for Sb(V) reduction remain largely uncharacterized. Inspired by the recently reported Sb(V) reductase belonging to the dimethyl sulfoxide reductase (DMSOR) family, this study was undertaken to use metagenomics and metatranscriptomics to unravel whether any DMSOR family genes in the bioreactor had the potential for Sb(V) reduction. A search through metagenomic-assembled genomes recovered from the microbial community found that some DMSOR family genes, designated sbrA (Sb(V) reductase gene), were highly transcribed in four phylogenetically disparate assemblies. The putative catalytic subunits were found to be representatives of two distinct phylogenetic clades of reductases that were most closely related to periplasmic nitrate reductases and respiratory arsenate reductases, respectively. Putative operons containing sbrA possessed many other components, including genes encoding c-type cytochromes, response regulators, and ferredoxins, which together implement Sb(V) reduction. This predicted ability was confirmed by incubating the enrichment culture with 13C-labeled CH4 and Sb(V) in serum bottles, where Sb(V) was reduced coincident with the production of 13C-labeled CO2. Overall, these results increase our understanding of how Sb(V) can be bio-reduced in environments.

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Data availability

All raw Illumina metagenomic sequence data were submitted to the Short Read Archive under accession number SRR8654052 for the first sample and SRR8668314 for another one. All raw metatranscriptomic sequence data were submitted to the Short Read Archive under accession number SRR8654739.

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Funding

The authors received financial support from the “National Key Technology R&D Program (2018YFC1802203),” the “National Natural Science Foundation of China (Grant No. 51878596, 21577123),” and the “Natural Science Funds for Distinguished Young Scholar of Zhejiang Province (LR17B070001).”

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Correspondence to He-Ping Zhao.

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Shi, LD., Wang, M., Han, YL. et al. Multi-omics reveal various potential antimonate reductases from phylogenetically diverse microorganisms. Appl Microbiol Biotechnol 103, 9119–9129 (2019). https://doi.org/10.1007/s00253-019-10111-x

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Keywords

  • Antimonate reduction
  • Molybdenum-containing
  • Dimethyl sulfoxide reductase family
  • Methane oxidation