A new class of OLD family ATPases functions in cell cycle progression in thermoacidophilic archaea

Overcoming lysogenization defect (OLD) proteins are diverse ATPases-nucleases functioning in antiphage defense in bacteria. However, the role of these proteins in archaea is currently unknown. Here, we describe a new class of archaeal OLD family ATPases and show that they are not involved in antiviral defense but play an essential role in cell cycle progression. We show that an OLD family enzyme of Saccharolobus islandicus REY15A (SisOLD) is essential for cell viability and exhibits cyclic expression patterns at both transcriptional and translational levels, displaying the peak expression during the genome synthesis (S) cell cycle phase. SisOLD overexpression or knockdown leads to significant growth retardation, cell size enlargement, and increased cellular DNA content. The ATPase activity but not the nickase activity of SisOLD is crucial for the normal cell cycle progression. Notably, SisOLD copurifies with chromatin-associated proteins, such as Cren7 and a histone deacetylase homolog, suggesting involvement in chromosome remodeling following its replication. Collectively our results suggest that SisOLD plays an important role in chromatin processing and remodeling, revealing a novel function of OLD family proteins.