CsmR is a novel transcriptional regulator in Haloferax volcanii linking motility and cell shape

Archaea rely on motility and morphological plasticity to navigate extreme environments, yet the transcriptional regulation of these processes remains poorly understood. In Haloferax volcanii, archaellation—the assembly of the rotary motility structure—is known to be transcriptionally controlled, but the key regulators have remained unidentified. Here, we show that CsmR is a novel transcriptional regulator that simultaneously controls archaellation and cell shape transitions in H. volcanii. Deletion of csmR results in the complete loss of motility and prevents rod-to-plate morphological switching, while overexpression leads to hypermotility and sustained rod-like morphology, demonstrating its central role in coordinating these processes. Comparative transcriptomics reveal that csmR deletion triggers widespread transcriptional changes, including the upregulation of archaellin and chemotaxis genes, suggesting direct regulatory control. Motif analysis identifies a conserved TATCA(N4)TGATA sequence upstream of regulated genes, supporting CsmR as a transcriptional regulator. Furthermore, csmR and cirA share extensive transcriptional overlap, with CirA likely fine-tuning CsmR-mediated regulation through post-translational modification. These findings establish CsmR as a key integrator of motility and morphological regulation, suggesting that haloarchaea coordinate these fundamental processes through a unified transcriptional network. Understanding this interplay provides new insights into archaeal adaptability and may reveal broader regulatory principles in prokaryotic cell biology.