The arbitrium system controls prophage induction

• Published in: Current biology Vol. 31; no. 22; pp. 5037 - 5045.e3
• Main Authors: Brady, Aisling, Quiles-Puchalt, Nuria, Gallego del Sol, Francisca, Zamora-Caballero, Sara, Felipe-Ruíz, Alonso, Val-Calvo, Jorge, Meijer, Wilfried J.J., Marina, Alberto, Penadés, José R.
• Format: Journal Article
• Language: English
• Published: England Elsevier Inc 22.11.2021; Cell Press
• Subjects: AimP; AimR; Bacillus Phages - genetics; Bacillus Phages - metabolism; bacteriophage; Bacteriophages - genetics; lysis; lysis/lysogeny; Lysogeny; Peptides - metabolism; phi3T; repressor; SOS response; SPβ phages; Virus Activation; SPβ phages; AimR; lysis/lysogeny; AimP; repressor; lysogeny; phi3T; SOS response; lysis; bacteriophage
• ISSN: 0960-9822; 1879-0445
• DOI: 10.1016/j.cub.2021.08.072

Some Bacillus-infecting bacteriophages use a peptide-based communication system, termed arbitrium, to coordinate the lysis-lysogeny decision. In this system, the phage produces AimP peptide during the lytic cycle. Once internalized by the host cell, AimP binds to the transcription factor AimR, reducing aimX expression and promoting lysogeny. Although these systems are present in a variety of mobile genetic elements, their role in the phage life cycle has only been characterized in phage phi3T during phage infection. Here, using the B. subtilis SPβ prophage, we show that the arbitrium system is also required for normal prophage induction. Deletion of the aimP gene increased phage reproduction, although the aimR deletion significantly reduced the number of phage particles produced after prophage induction. Moreover, our results indicated that AimR is involved in a complex network of regulation and brought forward two new players in the SPβ lysis-lysogeny decision system, YopN and the phage repressor YopR. Importantly, these proteins are encoded in an operon, the function of which is conserved across all SPβ-like phages encoding the arbitrium system. Finally, we obtained mutant phages in the arbitrium system, which behaved almost identically to the wild-type (WT) phage, indicating that the arbitrium system is not essential in the laboratory but is likely beneficial for phage fitness in nature. In support of this, by possessing a functional arbitrium system, the SPβ phage can optimize production of infective particles while also preserving the number of cells that survive after prophage induction, a strategy that increases phage persistence in nature. [Display omitted] •The arbitrium system controls prophage induction in B. subtilis•An operon downstream of the arbitrium system is involved in controlling lysogeny•The operon is functionally conserved in SPβ-like phages encoding arbitrium systems•YopR acts as the phage repressor in SPβ Bacillus subtilis phages from the SPβ family use the arbitrium system to communicate during infection of the host. Brady et al. show that this system is also required for induction of the resident prophage after activation of the host SOS response and identify a key operon involved in the control of the lytic/lysogenic cycle.