A novel RHH family transcription factor aCcr1 and its viral homologs dictate cell cycle progression in archaea

Abstract

Cell cycle regulation is of paramount importance for all forms of life. Here we report that a transcription factor and its viral homologs control cell division in Sulfolobales. The 58-aa-long RHH (ribbon-helix-helix) family protein (designated as aCcr1) is conserved in Crenarchaeota and diverse Sulfolobales viruses. aCcr1 is essential for cell viability of Saccharolobus islandicus REY15A (formally Sulfolobus islandicus REY15A) and exhibits a cyclic transcription pattern, with the highest level being reached during active cell division (D-phase), subsequent to the expression of CdvA, an archaea-specific cell division protein. Cells over-expressing cellular aCcr1 as well as the homologs encoded by large spindle-shaped viruses Acidianus two-tailed virus (ATV) and Sulfolobus monocaudavirus 3 (SMV3) show significant growth retardation and cell division failure, manifested as enlarged cells with multiple chromosomes. aCcr1 over-expression results in downregulation of over a dozen of genes including the cdvA gene. A conserved motif, aCcr1-box, located between the TATA-binding box and the translation initiation site in the promoters of 13 out of the 17 repressed genes, is critical for the aCcr1 binding. The aCcr1-box is present in the promoters of cdvA genes across Sulfolobales, suggesting that aCcr1-mediated cdvA repression is an evolutionarily conserved mechanism by which archaeal cells dictate cytokinesis progression, whereas their viruses take advantage of this mechanism to manipulate the host cell cycle.

A clade of RHH proteins ubiquitous in Sulfolobales and their viruses regulates cell cycle progression

“…This work is published together with the study by Yang et al. ( 77 ) describing SiRe_0197, homolog of SiL_0190, as aCcr1 of S. islandicus REY15A. They identified and characterized aCcr1 of S. islandicus REY15A by investigating transcription regulators with cyclic transcriptional patterns and obtained similar results to ours.…”

Genomics, Transcriptomics, and Proteomics of SSV1 and Related Fusellovirus: A Minireview

“…It is noteworthy that around one-third of the genes in the core genome (5/17) are putative transcriptional regulators (A79, C80, C102, B115, and B129), and this holds true also for several genes of the shell- and cloud-genomes ( Figure 2 , green circles). These transcriptional factors have not been experimentally characterized, although a couple of studies address the role of regulators that do not belong to the core genes [ 33 , 42 , 43 , 44 , 45 , 46 , 47 ]. C80 is homologous to the host transcriptional regulator aCcr-1 (SSO_RS11690 in S. solfataricus P2), a global cell cycle regulator in the Sulfolobales.…”