Comparative genomics reveals Dehalogenimonas genome dynamics and evolutionary trajectories toward organohalide...

Dehalogenimonas spp. specialize in organohalide respiration, a metabolism that features reductive dehalogenase (RDase) as the key catalyst, yet their evolutionary history and adaptation to halogenated substrates are largely unknown. Here, we surveyed the respiratory gene modules in Dehalogenimonas and constructed a pangenome for this genus. Comparative analyses revealed a genus-wide trend of genome streamlining, marked by contraction of gene families for general cellular functions, alongside preferential expansion of RDase-coding rdhA genes. Pairwise collinearity analysis showed poorly conserved gene order, indicating extensive genome rearrangements during the diversification of Dehalogenimonas lineages. Despite such genomic plasticity, all Dehalogenimonas rdhA genes assigned a definitive function are organized into operons positioned immediately adjacent to a two-component regulatory system, indicating that their transcription is tightly coupled to environmental signal sensing. We also identified an ssrA-associated genomic island carrying the signature dcpA, providing strong evidence for a role of mobile genetic elements in facilitating the spread of dihaloelimination potential across Dehalogenimonas. Selection pressure analyses further indicated that dcpA has been shaped by episodic positive selection at specific codon sites, indicative of adaptive fine-tuning, whereas purifying selection across many codon sites removes deleterious mutations and preserves core RDase catalytic function. Collectively, these streamlined, mosaic genomes provide an integrated evolutionary view of metabolic specialization in Dehalogenimonas.IMPORTANCEOrganohalide-respiring bacteria (OHRB) contribute to the cleanup of persistent halogenated contaminants in subsurface environments. Members affiliated with the genus Dehalogenimonas represent a distinct OHRB phylotype and have attracted growing attention for their ability to detoxify a broad range of organohalides, including the carcinogen vinyl chloride. Compared with other well-characterized OHRB, the genome architecture and evolutionary history of Dehalogenimonas spp. remain poorly resolved at the genus scale. Here, we address this knowledge gap by establishing the first comparative genomic framework for Dehalogenimonas. Our analyses reveal genome streamlining associated with specialization in organohalide respiration across the genus. We also identify conserved mechanisms that govern the acquisition and transcriptional control of Dehalogenimonas reductive dehalogenase genes. Together, this work sheds light on how Dehalogenimonas lineages evolve, acquire, and regulate essential respiratory components, providing a foundation to better understand their divergence and guide the deployment of these keystone OHRB in bioremediation practices.