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Nematoda from the terrestrial deep subsurface of South Africa

Abstract

Since its discovery over two decades ago, the deep subsurface biosphere has been considered to be the realm of single-cell organisms, extending over three kilometres into the Earth’s crust and comprising a significant fraction of the global biosphere1,2,3,4. The constraints of temperature, energy, dioxygen and space seemed to preclude the possibility of more-complex, multicellular organisms from surviving at these depths. Here we report species of the phylum Nematoda that have been detected in or recovered from 0.9–3.6-kilometre-deep fracture water in the deep mines of South Africa but have not been detected in the mining water. These subsurface nematodes, including a new species, Halicephalobus mephisto, tolerate high temperature, reproduce asexually and preferentially feed upon subsurface bacteria. Carbon-14 data indicate that the fracture water in which the nematodes reside is 3,000–12,000-year-old palaeometeoric water. Our data suggest that nematodes should be found in other deep hypoxic settings where temperature permits, and that they may control the microbial population density by grazing on fracture surface biofilm patches. Our results expand the known metazoan biosphere and demonstrate that deep ecosystems are more complex than previously accepted. The discovery of multicellular life in the deep subsurface of the Earth also has important implications for the search for subsurface life on other planets in our Solar System.

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Figure 1: General morphology of H. mephisto.
Figure 2: Bayesian-interference 50%-majority-rule consensus phylogenies based on small-subunit rDNA data.

Accession codes

Primary accessions

GenBank/EMBL/DDBJ

Data deposits

Sequence information for H. mephisto has been deposited at GenBank under accession number GQ918144.

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Acknowledgements

G.B. is grateful to the University of Ghent for allowing a year-long sabbatical, and for grants from the FWO, BOF and UFS. We express our recognition of the support provided by Tau Tona gold mine (AngloGold Ashanti Limited), Driefontein gold mine (Gold Fields Limited), Beatrix gold mine (Gold Fields Limited), Zondereinde mine (Northern Platinum Ltd) and Star Diamonds mine (Petra Diamonds), and by the many people without whom this work would have been impossible. In particular, we are grateful to F. Rheeder, H. Möller, T. Lineque, A. Thwala, K. Sokhela, C. Rose, R. Fynn, B. Visser, O. Holovachev, T. Moens, M. Couvreur and A. Vierstraete. We are grateful to E. Botes and K. Albertyn of the University of the Free State for their contributions to the data analysis. T.C.O. acknowledges support from a National Science Foundation Continental Dynamics Program grant (EAR 0409605). E.v.H. acknowledges support from a BioPAD/UFS Metagenomics Platform grant.

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A.G.-M., D.L. and W.B. all contributed equally to this study. G.B., A.G.-M., D.L., A.B. and M.E. collected the filtered samples and the control samples and performed field analyses. G.B. carried out the enrichments. A.G.-M. performed microbial DNA extraction and 16S rRNA amplification, sequencing and tree construction. C.M. performed DNA analyses on filters of mining water. W.B. provided the nematode identification, their morphological description and their molecular analyses. T.C.O. modelled the geochemical, 3H and 14C data. G.B. wrote the paper with input from W.B., A.G.-M., T.C.O. and E.v.H.

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Correspondence to G. Borgonie or T. C. Onstott.

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The authors declare no competing financial interests.

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This file contains Supplementary Figures 1-9 with legends. (PDF 1927 kb)

Supplementary Information

This file contains Supplementary Tables 1-5, Supplementary Methods, a Supplementary Discussion and additional references. (PDF 895 kb)

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Borgonie, G., García-Moyano, A., Litthauer, D. et al. Nematoda from the terrestrial deep subsurface of South Africa. Nature 474, 79–82 (2011). https://doi.org/10.1038/nature09974

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