Quorum sensing regulation in Erwinia carotovora affects development of Drosophila melanogaster infected larvae

Multi-host bacteria must rapidly adapt to drastic environmental changes, relying on integration of multiple stimuli for an optimal genetic response.Erwinia spp.are phytopathogens that cause soft-rot disease in plants.Erwinia carotovora Ecc15is used as a model for bacterial oral-route infection inDrosophila melanogasteras it harbors a gene, theErwiniavirulence factor (Evf), which has been previously shown to be a major determinant for infection ofD. melanogastergut. However, the factors involved in regulation ofevfexpression are poorly understood. We investigated whetherevfcould be controlled by quorum sensing since, in theErwiniagenus, quorum sensing regulates pectolytic enzymes, the major virulence factors needed to infect plants. Here, we show that transcription ofevfis positively regulated by quorum sensing inEcc15 viathe acyl-homoserine lactone (AHL) signal synthase ExpI, and the AHL receptors ExpR1 and ExpR2. Moreover, we demonstrate that the GacS/A two-component system is partially required forevfexpression. We also show that the load ofEcc15in the gut depends upon the quorum sensing-mediated regulation ofevf. Furthermore, we demonstrate that larvae infected withEcc15suffer a developmental delay as a direct consequence of the regulation ofevf viaquorum sensing. Overall, our results show thatEcc15relies on quorum sensing to control production of both pectolytic enzymes and Evf. This regulation influences the interaction ofEcc15with its two known hosts, indicating that quorum sensing and GacS/A signaling systems may impact bacterial disseminationviainsect vectors that feed on rotting plants.SignificanceIntegration of genetic networks allows bacteria to rapidly adapt to changing environments. This is particularly important in bacteria that interact with multiple hosts.Erwinia carotovora Ecc15is a plant pathogen that usesDrosophila melanogasteras a vector. To interact with these two hosts,Ecc15uses two different sets of virulence factors: plant cell wall-degrading enzymes to infect plants and theErwiniavirulence factor (evf) to infectDrosophila. Our work shows that, despite the virulence factors being different, both are regulated by homoserine lactone quorum sensing and the two component GacS/A system. Moreover, we show that these pathways are essential forEcc15loads in the gut ofDrosophilaand that this interaction carries a cost to the vector in the form of a developmental delay. Our findings provide evidence for the importance of quorum sensing regulation in the establishment of multi-host interactions.