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Abstract
The nematode Halicephalobus mephisto was originally discovered inhabiting a deep terrestrial aquifer 1.3 km underground. H. mephisto can thrive under conditions of abiotic stress including heat and minimal oxygen, where it feeds on a community of both chemolithotrophic and heterotrophic prokaryotes in an unusual ecosystem isolated from the surface biosphere. Here we report the comprehensive genome and transcriptome of this organism, identifying a signature of adaptation: an expanded repertoire of 70 kilodalton heat-shock proteins (Hsp70) and avrRpt2 induced gene 1 (AIG1) proteins. The expanded Hsp70 genes are transcriptionally induced upon growth under heat stress, and we find that positive selection is detectable in several members of this family. We further show that AIG1 may have been acquired by horizontal gene transfer (HGT) from a rhizobial fungus. Over one-third of the genes of H. mephisto are novel, highlighting the divergence of this nematode from other sequenced organisms. This work sheds light on the genomic basis of heat tolerance in a complete subterrestrial eukaryotic genome.
Highlights
The nematode Halicephalobus mephisto was originally discovered inhabiting a deep terrestrial aquifer 1.3 km underground
Given that Benchmarking Universal Single Copy Orthologs (BUSCO)’s thresholds are established from eight nematode genes from Clades I, III, and V17, it may not be well suited to divergent Clade IV nematodes such as H. mephisto, since it scored the P. redivivus genome (98% complete18) as only 82.1% complete
avrRpt2 induced gene 1 (AIG1) was originally reported to be completely absent from nematodes[45], but by relaxing the statistical stringency we find a single copy of the domain (Y67D2.4) in C. elegans annotated as a homolog of human mitochondrial ribosome associated GTPase 1 (MTG1), suggesting a possible divergence and expansion of the GTPase superfamily in H. mephisto and other nematodes
Summary
The nematode Halicephalobus mephisto was originally discovered inhabiting a deep terrestrial aquifer 1.3 km underground. We report the comprehensive genome and transcriptome of this organism, identifying a signature of adaptation: an expanded repertoire of 70 kilodalton heat-shock proteins (Hsp70) and avrRpt[2] induced gene 1 (AIG1) proteins. The water is warm (37 °C), alkaline (pH 7.9), hypoxic (0.42–2.3 mg/L dissolved O2,), and rich in biogenic methane (CH4)[1,2,3] In spite of these challenging conditions, a thriving, complex microbial community exists in this extreme environment, including chemolithoautotrophic organisms that extract energy from the subterrestrial rock and fix inorganic carbon[2,4]. We perform comprehensive genomic and transcriptomic studies in H. mephisto, revealing the evolutionary adaptive response to a subterrestrial environment, including expanded gene families and patterns of expression under heat stress. Consistent with the genomic divergence of H. mephisto, this repetitive element repertoire appears extremely different from known elements, including many unique or novel repeat families needing further characterization, and a significant 23.3% remain unclassified by either algorithm (Table 2)
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