Abstract

Quorum sensing (QS) is a process of cell-to-cell communication that bacteria use to orchestrate collective behaviors. QS relies on the cell-density-dependent production, accumulation, and receptor-mediated detection of extracellular signaling molecules called autoinducers (AIs). Gram-negative bacteria commonly use N-acyl homoserine lactones (AHLs) as their AIs, and they are detected by LuxR-type receptors. Often, LuxR-type receptors are insoluble when not bound to a cognate AI. In this report, we show that LuxR-type receptors are encoded on phage genomes, and in the cases we tested, the phage LuxR-type receptors bind to and are solubilized specifically by the AHL AI produced by the host bacterium. We do not yet know the viral activities that are controlled by these phage QS receptors; however, our observations, coupled with recent reports, suggest that their occurrence is more widespread than previously appreciated. Using receptor-mediated detection of QS AIs could enable phages to garner information concerning the population density status of their bacterial hosts. We speculate that such information can be exploited by phages to optimize the timing of execution of particular steps in viral infection.IMPORTANCE Bacteria communicate with chemical signal molecules to regulate group behaviors in a process called quorum sensing (QS). In this report, we find that genes encoding receptors for Gram-negative bacterial QS communication molecules are present on genomes of viruses that infect these bacteria. These viruses are called phages. We show that two phage-encoded receptors, like their bacterial counterparts, bind to the communication molecule produced by the host bacterium, suggesting that phages can "listen in" on their bacterial hosts. Interfering with bacterial QS and using phages to kill pathogenic bacteria represent attractive possibilities for development of new antimicrobials to combat pathogens that are resistant to traditional antibiotics. Our findings of interactions between phages and QS bacteria need consideration as new antimicrobial therapies are developed.

Highlights

  • Quorum sensing (QS) is a process of cell-to-cell communication that bacteria use to orchestrate collective behaviors

  • In the eavesdropping case, which is most pertinent to the observations we report here, a vibriophage encodes a homolog of a Vibrio quorum sensing (QS) receptor/ transcription factor called VqmA

  • We focused on genes encoding N-acyl homoserine lactone (AHL)-binding LuxR-type receptors/transcription factors because they exist in thousands of sequenced genomes of Gram-negative bacteria, making them an recognizable type of QS AI-receptor pair

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Summary

Introduction

Quorum sensing (QS) is a process of cell-to-cell communication that bacteria use to orchestrate collective behaviors. This final result demonstrates that the luxR-containing contig encodes a functional replication gene for a plasmid-like element, which is the reported state in which ⌽ARM81ld exists when it lysogenizes its Aeromonas host (6). ARM81 bacterial hosts share more than 90% identity, and yet the corresponding phage-encoded receptors LuxRApop and LuxR⌽ARM81ld, respectively, are only ϳ60% identical to one another (Fig. 2A; see Fig. S2B and S2C).

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