Acyl-Homoserine Lactones Can Induce Virus Production in Lysogenic Bacteria: an Alternative Paradigm for Prophage Induction

Abstract

Prophage typically are induced to a lytic cycle under stressful environmental conditions or when the host's survival is threatened. However, stress-independent, spontaneous induction also occurs in nature and may be cell density dependent, but the in vivo signal(s) that can trigger induction is unknown. In the present study, we report that acyl-homoserine lactones (AHL), the essential signaling molecules of quorum sensing in many gram-negative bacteria, can trigger phage production in soil and groundwater bacteria. This phenomenon also was operative in a lysogen of Escherichia coli. In model coculture systems, we monitored the real-time AHL production from Pseudomonas aeruginosa PAO1 using an AHL bioluminescent sensor and demonstrated that -prophage induction in E. coli was correlated with AHL production. As a working model in E. coli, we show that the induction responses of with AHL remained unaffected when recA was deleted, suggesting that this mechanism does not involve an SOS response. In the same lysogen we also demonstrated that sdiA, the AHL receptor, and rcsA, a positive transcriptional regulator of exopolysaccharide synthesis, are involved in the AHL-mediated induction process. These findings relate viral reproduction to chemical signals associated with high host cell abundance, suggesting an alternative paradigm for prophage induction.

Temperate phages both mediate and drive adaptive evolution in pathogen biofilms

“…Second, we compared the rates of spontaneous phage lysis of ɸ4 lysogens constructed in both the PAO1 and PAO1ΔlasR backgrounds: there was no significant difference in production of free phages in stationary phase cultures (median free phage density: PAO1, 3.4 × 10 8 pfu/mL, PAO1ΔlasR, 3.3 × 10 8 pfu/mL; Mann-Whitney test; W = 92.0, P = 0.345). Thus, although direct interaction between temperate phages and bacterial QS has been reported in other systems, via QS induced lysis by phages (39) or QS mediated alteration of phage receptor expression by bacteria (40), this does not appear to be an important factor in our study. Phages may have simply increased the supply of large effect mutations available to natural selection, notably via ɸ4 prophage integrations into mvfR (Fig.…”

The Accessory Genome of Pseudomonas aeruginosa

“…In contrast, several well-characterized conditions, such as mitomycin C treatment, use of antibiotics, UV light, and physiological stresses (e.g., amino acid deprivation), are known to promote mobilization of prophage accessory elements. Additionally, it was recently demonstrated that phage production by P. aeruginosa in soil and groundwater can be triggered by acyl-homoserine lactone quorum-sensing signal molecules (73). Thus, phage-mediated HGT may occur in a microbial population density-dependent manner, consistent with the prevailing thought that high bacterial density niches such as biofilms are rich environments for HGT (202).…”

Within-host competition determines reproductive success of temperate bacteriophages

“…Multiple infections in temperate phages have received some attention and the fitness consequences for individual phages have been addressed (Boyd and Bidwell, 1962;Serra-Moreno et al, 2008), but never in the context of prophage induction. Recently, it has been shown that prophage induction can occur in response to changes in bacterial density and it has been proposed that it is more than an adaptation to escape from a cell bound to die (Ghosh et al, 2009). The ability of prophages to respond to changes in transmission opportunities emphasizes The results herein emphasize the importance of multiple infections for natural phage populations, as they clearly show that lytic productivity of prophages declines, often substantially, when a host is shared between phages.…”

“…This changes once host DNA has been damaged. The bacterial stress response and possibly other signals can trigger the induction of the prophage, which then enters lytic development and finally lyses the host cell (Ptashne, 2004;Shkilnyj and Koudelka, 2007;Ghosh et al, 2009).…”