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A ubiquitous thermoacidophilic archaeon from deep-sea hydrothermal vents

Abstract

Deep-sea hydrothermal vents are important in global biogeochemical cycles, providing biological oases at the sea floor that are supported by the thermal and chemical flux from the Earth's interior. As hot, acidic and reduced hydrothermal fluids mix with cold, alkaline and oxygenated sea water, minerals precipitate to form porous sulphide–sulphate deposits. These structures provide microhabitats for a diversity of prokaryotes that exploit the geochemical and physical gradients in this dynamic ecosystem1. It has been proposed that fluid pH in the actively venting sulphide structures is generally low (pH < 4.5)2, yet no extreme thermoacidophile has been isolated from vent deposits. Culture-independent surveys based on ribosomal RNA genes from deep-sea hydrothermal deposits have identified a widespread euryarchaeotal lineage, DHVE2 (deep-sea hydrothermal vent euryarchaeotic 2)3,4,5,6. Despite the ubiquity and apparent deep-sea endemism of DHVE2, cultivation of this group has been unsuccessful and thus its metabolism remains a mystery. Here we report the isolation and cultivation of a member of the DHVE2 group, which is an obligate thermoacidophilic sulphur- or iron-reducing heterotroph capable of growing from pH 3.3 to 5.8 and between 55 and 75 °C. In addition, we demonstrate that this isolate constitutes up to 15% of the archaeal population, providing evidence that thermoacidophiles may be key players in the sulphur and iron cycling at deep-sea vents.

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Figure 1: Phylogenetic relationships between 16S rRNA sequences from strain T469 and representatives of the DHVE2 and Euryarchaeota.
Figure 2: Electron photomicrographs of T469.

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Acknowledgements

We thank the crew of the RV Melville, RV Atlantis and the DSROV Jason II and DSV Alvin teams for their assistance. This work is funded by the US National Science Foundation (A.-L.R., M.K.T, K.L.V.D.), a PSU Faculty Enhancement Award (A.-L. R.), the Natural Science and Engineering Research Council of Canada (NSERC), the US Department of Energy (T.J.B.), the US National Research Program, Water Resources Division, USGS, and NASA Exobiology (M.A.V.). We thank D. Moyles and R. Harris for technical help with TEM; P. Craddock for XRD; M. Baas and E. Hopmans for analytical assistance with the lipid analyses; I. Cozzarelli, M. Doughten and J. Jaeschke for the organic acid analysis; G. Sincerny, A. O'Neill and D. Decker for their assistance; and I. Ferrera for sharing qPCR results. J. Euzeby and M. Bartlett are acknowledged for assistance with naming the new archaeon. Author Contributions A.-L. R. and Y.L. isolated and characterized the acidophile; A.B.B. did all molecular phylogenetic and environmental DNA analyses; M.A.V. and J.D.K. did the qPCR analysis; T.J.B. did the ultrastructure analysis and interpretation; S.S. performed membrane lipid analysis; M.K.T. provided XRD data and geochemical interpretation; and K.L.V.D. provided samples, data on the sample locations and geochemical context. All authors discussed the results and commented on the manuscript.

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Correspondence to Anna-Louise Reysenbach.

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Reprints and permissions information is available at npg.nature.com/reprintsandpermissions. The new sequences described in this manuscript have been deposited in GenBank, accession numbers DQ451875 (T469) and DQ451876 (T449). The authors declare no competing financial interests.

Supplementary information

Supplementary Notes

This file contains the Supplementary Methods and Supplementary Tables 1–3, Supplementary Figures 1–3 and additional references. (PDF 302 kb)

Supplementary Figure 2

This is a high resolution version of Supplementary Figure 2. Example of a vent deposit from Mariner deep-sea vents (22°10.82'S, 176°36.09'W) and the outer accumulations of iron-oxide and sulphur biofilms typically where DHVE2 are detected. (PDF 304 kb)

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Reysenbach, AL., Liu, Y., Banta, A. et al. A ubiquitous thermoacidophilic archaeon from deep-sea hydrothermal vents. Nature 442, 444–447 (2006). https://doi.org/10.1038/nature04921

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