Energy conservation via organohalide respiration (OHR), comprising the reductive dehalogenation of halogenated organic compounds, is an inducible process in OHR capable Sulfurospirillum species. This work adds a first global RNA sequence of the well-studied Sulfurospirillum multivorans, a proteome and an acetylome of Sulfurospirillum halorespirans and two new Sulfurospirillum genomes that enlarge the repertoire of omics data allowing for future comparative analyses of organohalide-respiring bacteria. The differential RNA sequencing allowed for the identification of eight transcriptional units forming the tetrachloroethene regulon. A two-component system involved in tetrachloroethene signal transduction has been unambiguously identified in vivo and in vitro. The respective OmpR-family response regulator was functionally characterized. The results emphasize its role in promoting different transcriptional activation mechanisms induced by binding a cis-regulatory element containing a consensus sequence identified as a direct CTATW repeat separated by 17 bp. In S.multivorans, OHR is also subject to a unique memory effect in terms of a long-term transcriptional downregulation of the genes involved in OHR. This retentive memory effect in OHR gene regulation is now identified in a second species (S.halorespirans) suggesting a broader distribution of this regulatory phenomenon. Both acetylation pattern of the two-component system and the amount of bioavailable norcobamide cofactor were identified as potential factors affecting the memory effect. This study represents a major step towards the elucidation of the regulatory network controlling OHR gene expression in Sulfurospirillum species and might aid investigation of OHR regulation in other bacteria as well. Additionally, the first published acetylome of Campylobacterota helps to study other ecologically or medically important species of this clade.