The DSF Quorum Sensing System Controls the Positive Influence of Stenotrophomonas maltophilia on Plants

The interaction of the Gram-negative bacterium Stenotrophomonas maltophilia with eukaryotes can improve overall plant growth and health, but can also cause opportunistic infections in humans. While the quorum sensing molecule DSF (diffusible signal factor) is responsible for the regulation of phenotypes in pathogenic Stenotrophomonas, up until now, no beneficial effects were reported to be controlled by it. Our objective was to study the function of DSF in the plant growth promoting model strain S. maltophilia R551-3 using functional and transcriptomic analyses. For this purpose, we compared the wild-type strain with a mutant deficient in the rpfF (regulation of pathogenicity factors) gene that is essential for the synthesis of DSF. Oilseed rape seeds treated with the wild-type strain showed a statistically significant increase in germination rate compared with those treated with the rpfF mutant. Similarly, the wild-type strain exhibited better plant growth promotion and a greater efficiency in colonizing oilseed rape compared to the mutant strain. Moreover, only the wild-type was capable of forming structured cell aggregates both in vitro and in the rhizosphere, a characteristic mediated by DSF. Gene transcription analyses showed that numerous genes known to play a role in plant colonization (e.g. chemotaxis, cell motility, biofilm formation, multidrug efflux pumps) are controlled by the rpf/DSF system in S. maltophilia. In addition, we detected new potential functions of spermidine, primarily for both growth promotion and stress protection. Overall, our results showed a correspondence between the regulation of DSF and the positive interaction effect with the plant host.革兰氏阴性菌嗜麦芽窄食单胞菌（Stenotrophomonas maltophilia）与真核生物的相互作用，既可促进植物整体生长与健康，也可引发人类机会性感染。群体感应分子弥散信号因子（diffusible signal factor，以下简称DSF）是调控致病性嗜麦芽窄食单胞菌表型的关键因子，但迄今为止尚未见其介导有益生理效应的相关报道。本研究旨在通过功能实验与转录组分析，解析DSF在植物促生模式菌株嗜麦芽窄食单胞菌R551-3中的功能。为此，我们将野生型菌株与DSF合成必需的rpfF基因（致病性因子调控，regulation of pathogenicity factors）缺陷型突变株进行对照实验。经野生型菌株处理的油菜种子，其发芽率较rpfF突变株处理组呈现统计学意义上的显著提升。同理，相较于突变株，野生型菌株表现出更优异的植物促生效果，以及更强的油菜定殖能力。此外，仅野生型菌株可在体外与根际环境中形成结构化细胞聚集体，这一特性由DSF介导。基因转录分析显示，众多已知参与植物定殖过程的基因（如趋化性、细胞运动、生物膜形成、多药外排泵相关基因）均受嗜麦芽窄食单胞菌rpf/DSF系统调控。此外，本研究还发现了亚精胺的新型潜在功能，主要涉及生长促进与胁迫保护两大方面。综上，本研究结果证实，DSF的调控作用与嗜麦芽窄食单胞菌对植物宿主的正向互作效应密切相关。