A Function of SmeDEF, the Major Quinolone Resistance Determinant of Stenotrophomonas maltophilia, Is the Colonization of Plant Roots
ABSTRACTQuinolones are synthetic antibiotics, and the main cause of resistance to these antimicrobials is mutation of the genes encoding their targets. However, in contrast to the case for other organisms, such mutations have not been found in quinolone-resistantStenotrophomonas maltophiliaisolates, in which overproduction of the SmeDEF efflux pump is a major cause of quinolone resistance. SmeDEF is chromosomally encoded and highly conserved in all studiedS. maltophiliastrains; it is an ancient element that evolved over millions of years in this species. It thus seems unlikely that its main function would be resistance to quinolones, a family of synthetic antibiotics not present in natural environments until the last few decades. Expression of SmeDEF is tightly controlled by the transcriptional repressor SmeT. Our work shows that plant-produced flavonoids can bind to SmeT, releasing it fromsmeDEFandsmeToperators. Antibiotics extruded by SmeDEF do not impede the binding of SmeT to DNA. The fact that plant-produced flavonoids specifically inducesmeDEFexpression indicates that they arebona fideeffectors regulating expression of this resistance determinant. Expression of efflux pumps is usually downregulated unless their activity is needed. SincesmeDEFexpression is triggered by plant-produced flavonoids, we reasoned that this efflux pump may have a role in the colonization of plants byS. maltophilia. Our results showed that, indeed, deletion ofsmeEimpairsS. maltophiliacolonization of plant roots. Altogether, our results indicate that quinolone resistance is a recent function of SmeDEF and that colonization of plant roots is likely one original function of this efflux pump.