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<i>Pseudothermotoga elfii</i> strain DSM9442 and <i>P. elfii</i> subsp. <i>lettingae</i> strain DSM14385 are hyperthermophilic bacteria. <i>P. elfii</i> DSM9442 is a piezophile and was isolated from a depth of over 1600 m in an oil-producing well in Africa. <i>P. elfii</i> subsp. <i>lettingae</i> is piezotolerant and was isolated from a thermophilic bioreactor fed with methanol as the sole carbon and energy source. In this study, we analyzed both strains at the genomic and transcriptomic levels, paying particular attention to changes in response to pressure increases. Transcriptomic analyses revealed common traits of adaptation to increasing hydrostatic pressure in both strains, namely, variations in transport membrane or carbohydrate metabolism, as well as species-specific adaptations such as variations in amino acid metabolism and transport for the deep <i>P. elfii</i> DSM9442 strain. Notably, this work highlights the central role played by the amino acid aspartate as a key intermediate of the pressure adaptation mechanisms in the deep strain <i>P. elfii</i> DSM9442. Our comparative genomic and transcriptomic analysis revealed a gene cluster involved in lipid metabolism that is specific to the deep strain and that was differentially expressed at high hydrostatic pressures and might, thus, be a good candidate for a piezophilic gene marker in <i>Pseudothermotogales</i>.