The role of quorum-sensing system in the Sinorhizobium meliloti-alfalfa symbiosis

The term quorum sensing refers to the ability of bacteria to exhibit coordinated behavior in response to a particular population density. These bacteria rely on the production, accumulation, and subsequent response to diffusible signal molecules called autoinducers. These signal molecules collect in environments that can sustain a sufficiently dense population or "quorum" of the signal-producing bacteria. When the concentration of the signal molecule reaches a critical level, the bacterial population responds through the concerted expression of specific target genes. A variety of bacterial functions such as exopolysaccharide synthesis, motility, biofilm formation, and virulence are tightly controlled by quorum sensing in an array of symbiotic and pathogenic organisms. In this work we have performed a comprehensive examination of the ExpR/Sin quorum-sensing system of the gram-negative soil bacterium Sinorhizobium meliloti, an organism that forms a nitrogen-fixing symbiosis with its host plant Medicago sativa (alfalfa). By comparing the whole-genome expression profiles between a wild-type strain versus mutants missing one of the quorum-sensing regulatory components, we have outlined the regulatory map of the genes controlled by the ExpR/Sin system throughout the different stages of the free-living bacterial growth cycle, as well as once the bacteria establishes its symbiotic partnership with the host. We discovered that the transcriptional regulator ExpR is exceptionally versatile with the ability to regulate gene expression differentially in the presence and in the absence of the quorum sensing signal molecules. We demonstrated that the ExpR/Sin quorum-sensing system controls multiple bacterial phenotypes that are essential for its interaction with the host, such as motility, the synthesis of exopolysaccharides and the production of three novel calcium-binding proteins. Moreover, we provided mechanistic details of the population density-dependent regulation of flagella synthesis and presented an explanation for the inability of an autoinducer mutant to repress flagella synthesis at high-cell-population densities, leading to a decrease in plant invasion. Our work also showed that once the invasion occurs, quorum-sensing system is turned off inside the host and does not play a further role in gene regulation. Therefore, quorum sensing in S. meliloti plays a critical role in ensuring a successful plant-bacterial interaction.