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The initiation of bacterial chromosomal replication is regulated by multiple pathways. To explore novel regulators, we isolated multicopy suppressors for the cold-sensitive  hda-185  Δ sfiA(sulA)  mutant. Hda is crucial for the negative regulation of the initiator DnaA and the  hda-185  mutation causes severe replication overinitiation at the replication origin  oriC . The SOS-associated division inhibitor SfiA inhibits FtsZ ring formation, an essential step for cell division regulation during the SOS response, and Δ sfiA  enhances the cold sensitivity of  hda-185  cells in colony formation. One of the suppressors comprised the  yfdQ - yfdR - yfdS - yfdT  gene cluster carried on a cryptic prophage. Increased copy numbers of  yfdQRT  or  yfdQRS  inhibited not only  hda-185- dependent overinitiation, but also replication overinitiation in a hyperactive  dnaA  mutant, and in a mutant lacking an  oriC -binding initiation-inhibitor SeqA. In addition, increasing the copy number of the gene set inhibited the growth of cells bearing specific, initiation-impairing  dnaA  mutations. In wild-type cells, multicopy supply of  yfdQRT  or  yfdQRS  also inhibited replication initiation and increased hydroxyurea (HU)-resistance, as seen in cells lacking DiaA, a stimulator of DnaA assembly on  oriC . Deletion of the  yfdQ - yfdR - yfdS - yfdT  genes did not affect either HU resistance or initiation regulation. Furthermore, we found that DnaA bound specifically to YfdR in soluble protein extracts oversupplied with YfdQRST. Purified YfdR also bound to DnaA, and DnaA Phe46, an amino acid residue crucial for DnaA interactions with DiaA and DnaB replicative helicase was important for this interaction. Consistently, YfdR moderately inhibited DiaA-DnaA and DnaB-DnaA interactions. In addition, protein extracts oversupplied with YfdQRST inhibited replication initiation  in vitro . Given the roles of  yfdQ  and  yfdS  in cell tolerance to specific environmental stresses, the  yfdQ - yfdR - yfdS - yfdT  genes might downregulate the initiator DnaA- oriC  complex under specific growth conditions.

frontiers in microbiology

The Escherichia coli Cryptic Prophage Protein YfdR Binds to DnaA and Initiation of Chromosomal Replication Is Inhibited by Overexpression of the Gene Cluster yfdQ-yfdR-yfdS-yfdT