Abstract
Temperate phages have the ability to maintain their genome in their host, a process called lysogeny. For most, passive replication of the phage genome relies on integration into the host's chromosome and becoming a prophage. Prophages remain silent in the absence of stress and replicate passively within their host genome. However, when stressful conditions occur, a prophage excises itself and resumes the viral cycle. Integration and excision of phage genomes are mediated by regulated site-specific recombination catalyzed by tyrosine and serine recombinases. In the KplE1 prophage, site-specific recombination is mediated by the IntS integrase and the TorI recombination directionality factor (RDF). We previously described a sub-family of temperate phages that is characterized by an unusual organization of the recombination module. Consequently, the attL recombination region overlaps with the integrase promoter, and the integrase and RDF genes do not share a common activated promoter upon lytic induction as in the lambda prophage. In this study, we show that the intS gene is tightly regulated by its own product as well as by the TorI RDF protein. In silico analysis revealed that overlap of the attL region with the integrase promoter is widely encountered in prophages present in prokaryotic genomes, suggesting a general occurrence of negatively autoregulated integrase genes. The prediction that these integrase genes are negatively autoregulated was biologically assessed by studying the regulation of several integrase genes from two different Escherichia coli strains. Our results suggest that the majority of tRNA-associated integrase genes in prokaryotic genomes could be autoregulated and that this might be correlated with the recombination efficiency as in KplE1. The consequences of this unprecedented regulation for excisive recombination are discussed.
Highlights
Temperate bacteriophages are characterized by their ability to maintain their genome into the host, a process called lysogeny
These transcription start sites are correctly located relative to the s70-RNA polymerase holoenzyme binding sites, and the A at position 2464537 is perfectly positioned relative to the 210 box [35]. This latter transcription start site was detected in a genome-scale analysis of transcription in E. coli [36]
Based on our experimental model, we proposed that STI and OD shapes should be subjected to autoregulation, since in these cases the integrase gene promoter overlaps with the recombination region, whereas SIT and OC shapes should show integrase gene expression independent of the integrase protein
Summary
Temperate bacteriophages are characterized by their ability to maintain their genome into the host, a process called lysogeny. Most temperate phages integrate their genome into the host’s chromosome, becoming prophages. Circularized phage genomes are maintained as episomes. The so-called prophage is stable and replicates passively with its host genome. This situation can continue as long as outside conditions do not become threatening for the host, and for the virus. Once the prophage is induced, the process of lysogeny escape is engaged, and the phage enters a lytic mode of development [1]. A crucial event in this process is the excision of the prophage from the host’s chromosome. Excisive recombination is a highly regulated process that relies on two different levels of regulation: (i) protein activity, through the control of directionality by a recombination directionality factor (RDF), and (ii) protein synthesis via the coordinated expression of the integrase and RDF genes
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