Dissimilatory sulfate reduction in the archaeon ‘Candidatus Vulcanisaeta moutnovskia’ sheds light on the evolution of sulfur metabolism

• Published in: Nature Microbiology
• Main Authors: Chernyh, N. A., Neukirchen, Sinje, Frolov, Evgenii N., Sousa, Filipa L., Miroshnichenko, Margarita L., Merkel, Alexander Y., Pimenov, Nikolay V., Sorokin, Dimitry Y., Ciordia, Sergio, Mena, M. Carmen, Ferrer, Manuel, Golyshin, Peter N., Lebedinsky, A. V., Cardoso Pereira, Inês A., Bonch-Osmolovskaya, E. A.
• Other Authors: Russian Science Foundation, Ministry of Science and Higher Education of the Russian Federation, Instituto de Salud Carlos III, Biotechnology and Biological Sciences Research Council (UK), European Commission, European Research Council, Fundação para a Ciência e a Tecnologia (Portugal)
• Format: Article in Journal/Newspaper
• Language: unknown
• Published: Springer Nature 2020
• Subjects: Archaeal evolution; Evolution; Kamchatka Peninsula; Kamchatka
• Online Access: http://hdl.handle.net/10261/228930; https://doi.org/10.1038/s41564-020-0776-z; https://doi.org/10.13039/501100000781; https://doi.org/10.13039/501100001871; https://doi.org/10.13039/501100000268; https://doi.org/10.13039/501100006769; https://doi.org/10.13039/501100004587; https://doi.org/10.13039/501100000780

Dissimilatory sulfate reduction (DSR)—an important reaction in the biogeochemical sulfur cycle—has been dated to the Palaeoarchaean using geological evidence, but its evolutionary history is poorly understood. Several lineages of bacteria carry out DSR, but in archaea only Archaeoglobus, which acquired DSR genes from bacteria, has been proven to catalyse this reaction. We investigated substantial rates of sulfate reduction in acidic hyperthermal terrestrial springs of the Kamchatka Peninsula and attributed DSR in this environment to Crenarchaeota in the Vulcanisaeta genus. Community profiling, coupled with radioisotope and growth experiments and proteomics, confirmed DSR by ‘Candidatus Vulcanisaeta moutnovskia’, which has all of the required genes. Other cultivated Thermoproteaceae were briefly reported to use sulfate for respiration but we were unable to detect DSR in these isolates. Phylogenetic studies suggest that DSR is rare in archaea and that it originated in Vulcanisaeta, independent of Archaeoglobus, by separate acquisition of qmoABC genes phylogenetically related to bacterial hdrA genes. This work was supported by the Russian Science Foundation (grant number 17-74-30025) and in part by the grant from the Russian Ministry of Science and Higher Education (to N.A.C., A.V.L., E.N.F., M.L.M., A.Y.M., N.V.P. and E.A.B.-O.). Sequencing of PCR amplicons was performed using the scientific equipment of the core research facility ‘Bioengineering’ by T. Kolganova. The proteomics analysis was performed at the Proteomics Facility of the Spanish National Center for Biotechnology (CNB-CSIC), which belongs to ProteoRed, PRB2-ISCIII, supported by grant PT13/0001 (to S.C., M.C.M. and M.F.). P.N.G. acknowledges funding from the UK Biotechnology and Biological Sciences Research Council (BBSRC) within the ERA NET-IB2 programme, grant number ERA-IB-14-030 and the European Union Horizon 2020 Research and Innovation programme (Blue Growth: Unlocking the Potential of Seas and Oceans) under grant agreement number 634486, as ...