Since its discovery over two decades ago, the deep subsurface biosphere has been considered to be the realm of single cell organisms, extending >3 km into the Earth's crust and comprising a significant fraction of the global biosphere 1,2,3,4 . The constraints of temperature, energy, O 2 and space seemed to preclude the possibility of more complex multi-cellular 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 km deep fracture water encountered 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. 14 C data indicate that the fracture water in which the nematodes reside is 3-12 kyr old paleometeoric 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 upon 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 multi-cellular life in the deep subsurface of the Earth also has important implications for the search for subsurface life on other worlds in our solar system. . Halicephalobus mephisto

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BackgroundMany strains of Thermus have been isolated from hot environments around the world. Thermus scotoductus SA-01 was isolated from fissure water collected 3.2 km below surface in a South African gold mine. The isolate is capable of dissimilatory iron reduction, growth with oxygen and nitrate as terminal electron acceptors and the ability to reduce a variety of metal ions, including gold, chromate and uranium, was demonstrated. The genomes from two different Thermus thermophilus strains have been completed. This paper represents the completed genome from a second Thermus species - T. scotoductus.ResultsThe genome of Thermus scotoductus SA-01 consists of a chromosome of 2,346,803 bp and a small plasmid which, together are about 11% larger than the Thermus thermophilus genomes. The T. thermophilus megaplasmid genes are part of the T. scotoductus chromosome and extensive rearrangement, deletion of nonessential genes and acquisition of gene islands have occurred, leading to a loss of synteny between the chromosomes of T. scotoductus and T. thermophilus. At least nine large inserts of which seven were identified as alien, were found, the most remarkable being a denitrification cluster and two operons relating to the metabolism of phenolics which appear to have been acquired from Meiothermus ruber. The majority of acquired genes are from closely related species of the Deinococcus-Thermus group, and many of the remaining genes are from microorganisms with a thermophilic or hyperthermophilic lifestyle. The natural competence of Thermus scotoductus was confirmed experimentally as expected as most of the proteins of the natural transformation system of Thermus thermophilus are present. Analysis of the metabolic capabilities revealed an extensive energy metabolism with many aerobic and anaerobic respiratory options. An abundance of sensor histidine kinases, response regulators and transporters for a wide variety of compounds are indicative of an oligotrophic lifestyle.ConclusionsThe genome of Thermus scotoductus SA-01 shows remarkable plasticity with the loss, acquisition and rearrangement of large portions of its genome compared to Thermus thermophilus. Its ability to naturally take up foreign DNA has helped it adapt rapidly to a subsurface lifestyle in the presence of a dense and diverse population which acted as source of nutrients. The genome of Thermus scotoductus illustrates how rapid adaptation can be achieved by a highly dynamic and plastic genome.