Quorum-sensing quenching by rhizobacterial volatiles

Abstract

We show that volatile organic compounds (VOCs) produced by rhizospheric strains Pseudomonas fluorescens B-4117 and Serratia plymuthica IC1270 may act as inhibitors of the cell-cell communication quorum-sensing (QS) network mediated by N-acyl homoserine lactone (AHL) signal molecules produced by various bacteria, including strains of Agrobacterium, Chromobacterium, Pectobacterium and Pseudomonas. This quorum-quenching effect was observed when AHL-producing bacteria were treated with VOCs emitted by strains B-4117 and IC1270 or with dimethyl disulfide (DMDS), the major volatile produced by strain IC1270. LC-MS/MS analysis revealed that treatment of strains Pseudomonas chlororaphis 449, Pseudomonas aeruginosa PAO1 or Ps. fluorescens 2-79 with VOCs emitted by strain IC1270 or DMDS drastically decreases the amount of AHLs produced by these bacteria. Volatile organic compounds produced by Ps. chlororaphis 449 were able to suppress its own QS-induction activity, suggesting a negative interaction between VOCs and AHL molecules in the same strain. Quantitative RT-PCR analysis showed that treatment of Ps. chlororaphis 449 with VOCs emitted by cells of IC1270, B-4117 or 449 itself, or with DMDS, leads to significant suppression of transcription of AHL synthase genes phzI and csaI. Thus, along with AHLs, bacterial volatiles might be considered another type of signal molecule involved in microbial communication in the rhizosphere.

Volatile affairs in microbial interactions

“…For example, volatiles produced by S. plymuthica can inhibit cell-cell communication mediated by acyl homoserine lactone molecules in Agrobacterium, Pectobacterium and Pseudomonas. Volatiles emitted by S. plymuthica decreased the amount of acyl homoserine lactone produced by these bacteria, leading to significant suppression of transcription of acyl homoserine lactone synthase genes (Chernin et al, 2011).…”

“…The fact that the production of antibiotics in these bacteria is regulated by quorum sensing (QS) suggests that volatiles may interfere with bacterial cell-cell communication. Indeed, several studies revealed that volatiles can affect QS systems in bacteria, negatively or positively (Schulz et al, 2010;Chernin et al, 2011;Ahmad et al, 2014). For example, volatiles produced by S. plymuthica can inhibit cell-cell communication mediated by acyl homoserine lactone molecules in Agrobacterium, Pectobacterium and Pseudomonas.…”

Pseudomonas Strains Naturally Associated with Potato Plants Produce Volatiles with High Potential for Inhibition of Phytophthora infestans

“…Highly significant volatile-mediated effects of bacteria have been reported for various target organisms, including bacteria themselves (1)(2)(3)(4)(5), plants (5)(6)(7)(8)(9), and fungi (10)(11)(12). The research carried out to understand the nature of this volatile-mediated interaction of bacteria with plants and with other bacteria has focused so far on model organisms (e.g., Arabidopsis thaliana and Escherichia coli) and has enabled identification of some of the active compounds involved in the respective interactions, such as indole, 2,3-butanediol, dimethyl disulfide, hydrogen sulfide, and ammonia.…”

Mining into interspecific bacterial interactions

“…Volatiles exposed colonies showed reduced growth and white coloration indicating the lack of prodigiosin production. It is plausible that this observation is related to the inhibition of quorum sensing as previously reported by Moroshi and Chernin (Morohoshi et al, 2007;Chernin et al, 2011).…”

“…These physiochemical properties make volatiles ideal metabolites for communication and antagonistic interactions between soil microorganisms living at a certain distance from each other. Indeed, recent studies indicate that soil microorganisms can employ volatile compounds as info-chemicals, growth stimulants, growth inhibitors and inhibitors of quorum-sensing (Kai et al, 2009;Chernin et al, 2011;Effmert et al, 2012;Kim et al, 2013). Furthermore, rhizosphere bacteria emit volatiles that can promote plant growth and elicit induced systemic resistance (ISR) and induced systemic tolerance (IST) in plants (Ryu et al, 2003;Ryu et al, 2004).…”