Lytic gene expression in the temperate bacteriophage GIL01 is activated by a phage-encoded LexA homologue

Abstract

The GIL01 bacteriophage is a temperate phage that infects the insect pathogen Bacillus thuringiensis. During the lytic cycle, phage gene transcription is initiated from three promoters: P1 and P2, which control the expression of the early phage genes involved in genome replication and P3, which controls the expression of the late genes responsible for virion maturation and host lysis. Unlike most temperate phages, GIL01 lysogeny is not maintained by a dedicated phage repressor but rather by the host’s regulator of the SOS response, LexA. Previously we showed that the lytic cycle was induced by DNA damage and that LexA, in conjunction with phage-encoded protein gp7, repressed P1. Here we examine the lytic/lysogenic switch in more detail and show that P3 is also repressed by a LexA–gp7 complex, binding to tandem LexA boxes within the promoter. We also demonstrate that expression from P3 is considerably delayed after DNA damage, requiring the phage-encoded DNA binding protein, gp6. Surprisingly, gp6 is homologous to LexA itself and, thus, is a rare example of a LexA homologue directly activating transcription. We propose that the interplay between these two LexA family members, with opposing functions, ensures the timely expression of GIL01 phage late genes.

Role of plasmid plasticity and mobile genetic elements in the entomopathogen Bacillus thuringiensis serovar israelensis

“…3 ) (Fornelos, Bamford and Mahillon 2011 ; Fornelos et al. 2015 , 2018 ). The induction of the phage is SOS-dependent, but unlike phage lambda, it does not depend on a CI-like repressor.…”

“…Both promoters P1 and P3 are switch on by DNA damage, but P3 expression is delayed in comparison with P1 and requires a second small phage-encoded protein, gp6 (encoded by CDS 6) that is a LexA homologous (Fornelos et al. 2018 ). These recent findings indicate that upon DNA damage gp6 can directly activate transcription at P3 , resulting in the expression of late genes required for virion assembly and lysis of the host.…”

Comparative Analysis of Transcriptional Regulation Patterns: Understanding the Gene Expression Profile in Nucleocytoviricota

“…That may remain true for other NCLDVs and even their distant tectiviruses relatives. A transcription cascade model of gene expression has been evidenced for tectiviruses [ 74 ], reinforcing the hypothesis that the common ancestor of these viruses and NCLDVs already had that mechanism of gene regulation.…”

Genomic and Proteomic Characterization of Bacteriophage BH1 Spontaneously Released from Probiotic Lactobacillus rhamnosus Pen

“…These are involved in the SOS response, leading to the repair of single-stranded DNA [42]. It has also been shown that these proteins can indirectly influence the level of spontaneous prophage induction [17,43,44]. The next gene, similar to ORF27, is also transcribed leftward, and the protein encoded by this ORF presumably regulates the transcription of genes when there is cellular stress associated with DNA damage, which may be related to the genetic switch of phages from a lysogenic pathway to a lytic pathway [42,45].…”