Widespread Utilization of Peptide Communication in Phages Infecting Soil and Pathogenic Bacteria

Abstract

Graphical Abstract Highlights d Arbitrium-like systems are common in phages infecting pathogens and soil bacteria d Peptide-based arbitrium communication regulates lysogeny in numerous phage types d Arbitrium systems are frequently encoded on mobile pathogenicity elements d A peptide-responsive non-coding RNA controls the regulator of the lysogenic state Authors Avigail Stokar-Avihail, Nitzan Tal, Zohar Erez, Anna Lopatina, Rotem Sorek Correspondence rotem.sorek@weizmann.ac.il In Brief Stokar-Avihail et al. discovered that numerous types of phages and mobile genetic elements encode peptide-based communication systems that guide lysogeny decisions. These elements infect many soil and pathogenic Bacilli. Peptide-based lysogeny decisions are likely executed by a non-coding RNA that controls the regulator of lysogeny. SUMMARY Temperate phages can adopt either a lytic or lysogenic lifestyle within their host bacteria. It was recently shown that Bacillus-subtilis-infecting phages of the SPbeta group utilize a peptide-based communication system called arbitrium to coordinate the lysogeny decision. The occurrence of peptide-based communication systems among phages more broadly remains to be explored. Here, we uncover a wide array of peptide-based communication systems utilized by phages for lysogeny decisions. These arbitrium-like systems show diverse peptide codes and can be detected in numerous genetically distant phage types and conjugative elements. The pathogens Bacillus anthracis, Bacillus cereus, andBacillus thuringiensis are commonly infected by arbitrium-carrying mobile elements, which often carry toxins essential for pathogenicity. Experiments with phages containing these arbitrium-like systems demonstrate their involvement in lysogeny decisions. Finally, our results suggest that the peptidebased decision is executed by an antisense RNA that controls the regulator of the lysogenic state.

How repeated outbreaks drive the evolution of bacteriophage communication: Insights from a mathematical model

“…Hence, peptide communication is used to promote lysogeny when many infections have occurred. Similar arbitrium-like systems have now been found in a range of different phages [10]. Notably, these phages each use a slightly different signalling peptide, and do not seem to respond to the signals of other phages [9,10].The discovery of phage-encoded signalling peptides raises the question of how this viral communication system evolved.…”

“…Similar arbitrium-like systems have now been found in a range of different phages [10]. Notably, these phages each use a slightly different signalling peptide, and do not seem to respond to the signals of other phages [9,10].The discovery of phage-encoded signalling peptides raises the question of how this viral communication system evolved. While the arbitrium system has not yet been studied theoretically, previous work has considered the evolution of lysogeny and of other phage-phage interactions.…”

“…infects a host cell [9,10], each infection leads to an immediate increase of the arbitrium concentration A by an increment c. The lysis-lysogeny decision is effected by the current arbitrium concentration: a fraction ϕ(A) of the infections results in the production of a lysogen, while the remaining fraction (1 − ϕ(A)) results in a lytic infection. Arbitrium does not decay spontaneously in the model (since it is a small peptide, spontaneous extracellular degradation is considered to be negligible), but it is taken up by bacteria at a rate u (e.g., through general bacterial peptide importers such as OPP [9]), and then degraded intracellularly.…”

Peptide-based quorum sensing systems inPaenibacillus polymyxa

“…In B. thuringiensis the PlcR receptor is a transcription factor that becomes activated when bound to its cognate PapR peptide, leading to expression of virulence factors that facilitate infection of its insect larval host 27 . Such peptide-based communication was recently shown also to control the lysis-lysogeny decision of phages infecting many species of Bacillus 28,29 .…”

Prophage induction mediated by quorum sensing signals alters soil bacterial community structure

“…Communication among phages through phage-encoded arbitrium peptides was first described by Erez et al 13 , and the following studies 14,[24][25][26] revealed the molecular basis for the production, detection, and consequences of the short signaling peptides on phages lysogeny-lysis decisions.…”