Abstract

SummarySome 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.

Highlights

  • Deciphering the basis of communication is essential for understanding the communities where organisms live and their ecological behaviors

  • Analysis of aimR and aimP mutants SPb is one of the prophages present in the B. subtillis 168 strain and was selected as the phage model used to study the impact of the arbitrium system in prophage induction

  • Several studies have analyzed the transcriptomic landscape of this strain in response to different stimuli, including induction of the SOS response by treating the lysogenic cells with mitomycin C (MC).[7,8]

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Summary

Introduction

Deciphering the basis of communication is essential for understanding the communities where organisms live and their ecological behaviors. Quorum-sensing communication mechanisms in bacteriophages (phages)—such as the arbitrium system—to make lysis-lysogeny decisions represent a breakthrough confirming viruses as sophisticated social agents in the microbial world.[1,2] In addition, other social behaviors, such as cooperation, where different viruses co-infect a host,[3,4] or altruism to defeat the CRISPR-Cas-mediated immune defense of bacteria[5,6] confirm that viruses have different communication skills that may have a crucial role in establishing sophisticated social microbial networks. The novel arbitrium system was described in the Bacillus subtillis SPb group of phages using phi3T as a model. In this elegant system, phages communicate during the infection cycle using a six-amino-acid (aa) peptide (AimP) as a signal.[2] Depending on the concentration of peptide present, phages undergo either a lytic or lysogenic cycle.

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