Quorum-quenching limits quorum-sensing exploitation by signal-negative invaders

Authors: TANNIERES, MELANIE - European Biological Control Laboratory (EBCL); LANG, JULIEN - National Council For Scientific Research-Cnrs; BARNIER, CLAUDIE - National Council For Scientific Research-Cnrs; SHYKOFF, JACQUI - National Council For Scientific Research-Cnrs; FAURE, DENIS - National Council For Scientific Research-Cnrs

Submitted to: Scientific Reports
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 12/2/2016
Publication Date: 1/5/2017
Citation: Tannieres, M., Lang, J., Barnier, C., Shykoff, J., Faure, D. 2017. Quorum-quenching limits quorum-sensing exploitation by signal-negative invaders. Scientific Reports. 7:40126.

Interpretive Summary: Many types of bacteria can communicate between cells by quorum sensing (QS), which involves the production, diffusion and detection of chemical signaling compounds that can change the behavior of the bacteria. Thus, QS provides a mechanism for groups of bacterial cells to cooperate, which can lead to the production of biofilms, synthesis of antibiotics, increase of virulence, and transfer of plasmids (which can transfer genetic information between bacterial cells). However, as a social system, QS can be negatively affected by QS-cheating (cells that do not respond to the QS signal, but that benefit from those that do), and QS-hijacking (cells that use the QS-signals emitted by others to activate a different response that benefits only themselves). Agrobacterium tumefaciens cells can carry a tumour-inducing (Ti) plasmid that causes crown gall disease in their host plants. This plasmid has genes that control infection of the host plant and that induce the plant to produce opines, which nourish the bacteria. We conducted experiments that showed that the ability of A. tumefaciens to inactivate QS-signals by expressing QS-degrading enzyme could reduce the success of QS signal-negative Ti-plasmids, thus helping to reduce QS-cheating and QS-hijacking. Quorum sensing is a widespread mechanism used by many pathogenic bacteria to synchronize virulence factor production which has several levels of regulation, hence offering multiple targets for the development of new methods to control bacterial diseases which have a lower risk of resistance development compared to the use of antibiotics.

Technical Abstract: Some bacteria produce and perceive quorum-sensing (QS) signals that coordinate several behaviors, including the physiologically costly processes of exoenzyme production and plasmid transfer. In the case of plasmid transfer, the emergence of QS signal-altered invaders and their policing are poorly documented. In Agrobacterium tumefaciens, the virulence Ti-plasmid encodes both synthesis and sensing of QS-signals, which promote its transfer from a donor to a recipient cell. Here, we reported that QS-altered A. tumefaciens mutants arose during experimental evolution. All showed improved growth compared to their ancestor. Genome sequencing revealed that, though some had lost the Ti-plasmid, most were defective for QS-signal synthesis and Ti-plasmid conjugation (traR mutations) and one exhibited a QS-signal exploitation behaviour, using a signal produced by other cells to enhance its own Ti-plasmid transfer. We explored mechanisms that can limit this QS-hijacking. We showed that the A. tumefaciens capacity to inactivate QS-signals by expressing QS-degrading enzyme could attenuate dissemination of the QS signal-negative Ti-plasmids. This work shows that enzymatic QS disruption whether encoded by the QS-producing Ti-plasmid itself, by a companion plasmid in the same donor cells, or by one in the recipient cells, in all cases can serve as a mechanism for controlling QS exploitation by QS signal-negative mutants.