Horizontal gene transfer as a mechanism of adaptation to an extreme subterranean environment by the nematode Halicephalobus mephisto

Genetic signatures associated with adaptation to extreme conditions are of interest for understanding the limits of life on earth and in the search for extraterrestrial life, but animals (as opposed to bacteria or archaea) are relatively rare in extreme habitats. We have performed sequencing, protein prediction, and genomic analysis on a unique extremophile metazoan, Halicephalobus mephisto. H. mephisto is a nematode isolated from a borehole nearly a mile beneath the earth’s surface. There it experiences heat, low levels of oxygen, and extreme darkness, among other extreme features. Here we present data supporting an unusual evolutionary signature in its genome consistent with adaptation to an extreme environment.Specifically, a sixteen-nematode comparative analysis revealed an expanded repertoire of 70 kilodalton heat-shock protein (Hsp70) in H. mephisto, which contains 110 detected Hsp70 gene paralogs as compared to just 16 in C. elegans. In addition to a large number of Hsp70 proteins, we found evidence for several of these Hsp70 proteins being derived from bacterial sources, some of which are also extremophiles. Furthermore, we identified a 6-phosphogluconolactanse as being derived from bacterial sources as well. These data are consistent with horizontal gene transfer as a mechanism of animal adaptation of H. mephisto to the deep, hot terrestrial subsurface.