Abstract
Nitrifying microorganisms occur across a wide temperature range from 4 to 84 °C and previous studies in geothermal systems revealed their activity under extreme conditions. Archaea were detected to be responsible for the first step of nitrification, but it is still a challenging issue to clarify the identity of heat-tolerant nitrite oxidizers. In a long-term cultivation approach, we inoculated mineral media containing ammonium and nitrite as substrates with biofilms and sediments of two hot springs in Yellowstone National Park (USA). The nitrifying consortia obtained at 70 °C consisted mostly of novel Chloroflexi as revealed by metagenomic sequencing. Among these, two deep-branching novel Chloroflexi were identified as putative nitrite-oxidizing bacteria (NOB) by the presence of nitrite oxidoreductase encoding genes in their genomes. Stoichiometric oxidation of nitrite to nitrate occurred under lithoautotrophic conditions, but was stimulated by organic matter. Both NOB candidates survived long periods of starvation and the more abundant one formed miniaturized cells and was heat resistant. This detection of novel thermophilic NOB exemplifies our still incomplete knowledge of nitrification, and indicates that nitrite oxidation might be an ancient and wide-spread form of energy conservation.
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Data availability
Metagenomic and 16S rRNA gene amplicon sequence data are available in the European Nucleotide Archive (ENA) under accession number PRJEB28556. Requests for bacterial enrichment cultures are subject to the “General Permit Conditions” and cannot be shared by the authors without permission from U.S. National Park Service.
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Acknowledgements
The authors thank the National Park Service for permission to perform research in Yellowstone National Park (Permit YELL-2007-SCI-5698). Elke Woelken is acknowledged for excellent technical help in electron microscopy and Yvonne Bedarf and Christina Bietz for initial cultivation. We also thank Lia Burkhardt and Kerstin Reumann for sequencing assistance and we are grateful to Ilias Lagkouvardos and Antonios Kioukis for kindly enabling our analyses on the IMNGS platform.
Funding
This work was funded by the Deutsche Forschungsgemeinschaft (DFG, German Research Foundation grant SP 667/7-1+2) and the Netherlands Organization for Scientific Research (Grants 863.14.019, 016.Vidi.189.050 and SIAM Gravitation Grant 024.002.002).
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EB and JS performed sampling at YNP, ES, JH, SL designed research, ES, KW, JH, DI performed research, JH, MA, MS, JF, SL analyzed data, and ES, JH and SL wrote the paper. All authors read and agreed on the final paper.
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Spieck, E., Spohn, M., Wendt, K. et al. Extremophilic nitrite-oxidizing Chloroflexi from Yellowstone hot springs. ISME J 14, 364–379 (2020). https://doi.org/10.1038/s41396-019-0530-9
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DOI: https://doi.org/10.1038/s41396-019-0530-9
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