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Domestication of previously uncultivated Candidatus Desulforudis audaxviator from a deep aquifer in Siberia sheds light on its physiology and evolution

The ISME Journal (2019) | Download Citation

Abstract

An enigmatic uncultured member of Firmicutes, Candidatus Desulforudis audaxviator (CDA), is known by its genome retrieved from the deep gold mine in South Africa, where it formed a single-species ecosystem fuelled by hydrogen from water radiolysis. It was believed that in situ conditions CDA relied on scarce energy supply and did not divide for hundreds to thousand years. We have isolated CDA strain BYF from a 2-km-deep aquifer in Western Siberia and obtained a laboratory culture growing with a doubling time of 28.5 h. BYF uses not only H2 but also various organic electron donors for sulfate respiration. Growth required elemental iron, and ferrous iron did not substitute for it. A complex intracellular organization included gas vesicles, internal membranes, and electron-dense structures enriched in phosphorus, iron, and calcium. Genome comparison of BYF with the South African CDA revealed minimal differences mostly related to mobile elements and prophage insertions. Two genomes harbored <800 single-nucleotide polymorphisms and had nearly identical CRISPR loci. We suggest that spores with the gas vesicles may facilitate global distribution of CDA followed by colonization of suitable subsurface environments. Alternatively, a slow evolution rate in the deep subsurface could result in high genetic similarity of CDA populations at two sites spatially separated for hundreds of millions of years.

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Data availability

The annotated genome sequence of CDA strain BYF has been deposited in the NCBI GenBank database under the accession number CP034260. The Supplementary Information includes Supplementary Figures 1–4 and Supplementary Tables 1–4. Other data that support the findings of this study are available from the corresponding author upon request.

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Acknowledgements

Strain BYF isolation was supported by the Russian Foundation for Basic Research (grant # 18–04–00181) to O.V.K. group. Studies of strain BYF morphology and physiology were supported by the Russian Science Foundation (grant # 18-14-00130) to O.V.K. group. The work of N.V.R. group on sequencing and analysis of CDA genome was supported by the Russian Science Foundation (grant 14–14–01016) and the Ministry of Science and Higher Education of the Russian Federation. We thank Andrei Miller for his excellent assistance with TEM. We appreciate the three anonymous reviewers’ suggestions that helped to improve the manuscript.

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Affiliations

  1. Laboratory of Biochemistry and Molecular Biology, Tomsk State University, Tomsk, 634050, Russia

    • Olga V. Karnachuk
    • , Yulia A. Frank
    •  & Anastasia P. Lukina
  2. Institute of Bioengineering, Research Center of Biotechnology of the Russian Academy of Sciences, Moscow, 119071, Russia

    • Vitaly V. Kadnikov
    • , Alexey V. Beletsky
    • , Andrey V. Mardanov
    •  & Nikolai V. Ravin

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Contributions

O.V.K. and N.V.R. designed the study and wrote the manuscript. Y.A.F. and A.P.L. performed the research work on CDA isolation, cultivation, morphology, and physiology. A.V.M. and V.V.K. sequenced the genome of strain BYF and performed comparative genomics analysis. A.V.B. performed SNP analysis and genome comparisons. All authors commented on and approved the manuscript.

Conflict of interest

The authors declare that they have no conflict of interest.

Corresponding authors

Correspondence to Olga V. Karnachuk or Nikolai V. Ravin.

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https://doi.org/10.1038/s41396-019-0402-3