The LuxO-OpaR quorum-sensing cascade differentially controls Vibriophage VP882 lysis-lysogeny decision making in liquid and on surfaces

Abstract

Quorum sensing (QS) is a process of cell-to-cell communication that bacteria use to synchronize collective behaviors. QS relies on the production, release, and group-wide detection of extracellular signaling molecules called autoinducers (AIs). Vibrios use two QS systems: the LuxO-OpaR circuit and the VqmA-VqmR circuit. Both QS circuits control group behaviors including biofilm formation and surface motility. The Vibrio parahaemolyticus temperate phage {varphi}VP882 encodes a VqmA homolog (called VqmA{varphi}). When VqmA{varphi} is produced by {varphi}VP882 lysogens, it binds to the host-produced AI called DPO and launches the {varphi}VP882 lytic cascade. This activity times induction of lysis with high host cell density and presumably promotes maximal phage transmission to new cells. Here, we explore whether, in addition to induction from lysogeny, QS controls the initial establishment of lysogeny by {varphi}VP882 in naive host cells. Using mutagenesis, phage infection assays, and phenotypic analyses, we show that {varphi}VP882 connects its initial lysis-lysogeny decision to both host cell density and whether the host resides in liquid or on a surface. Only host cells in the low-density QS state undergo lysogenic conversion. The QS regulator LuxO[~]P promotes {varphi}VP882 lysogenic conversion of low cell density planktonic host cells. By contrast, the ScrABC surface-sensing system regulates lysogenic conversion of low cell density surface-associated host cells. ScrABC controls the abundance of the second messenger molecule cyclic diguanylate, which in turn, modulates motility. The scrABC operon is only expressed when its QS repressor, OpaR, is absent. Thus, at low cell density, QS-dependent derepression of scrABC drives lysogenic conversion in surface-associated host cells. These results demonstrate that {varphi}VP882 integrates cues from multiple sensory pathways into its lifestyle decision making upon infection of a new host cell. AUTHOR SUMMARYBacteria in nature often exist in surface-associated communities including sessile biofilms and highly motile swarms. Thus, bacteriophages can encounter their hosts in structured communities. Much bacteriophage research is performed in homogenous, planktonic cultures containing cells that neither display the gene expression patterns nor the behaviors that occur in surface communities. The Vibrio parahaemolyticus temperate phage {varphi}VP882, after lysogenizing its host, can monitor the vicinal cell density and time lytic induction with high host cell density. Here, we show that, upon infection of a new host cell, {varphi}VP882 assesses host cell density to make the decision whether to lyse or lysogenize. Only host cells at low density undergo lysogenic conversion, and the components driving the phage decision-making process vary depending on whether the host cell is in liquid or associated with a solid surface. We propose that by tuning its lysis-lysogeny decision making to both host cell density and the physical environment of the host, {varphi}VP882 can maximize transmission to new host cells and dispersal to new environments.