<i>Erwinia carotovora</i> Quorum Sensing System Regulates HostSpecific Virulence Factors and Development Delay in <i>Drosophila melanogaster</i>



Vieira, Filipe JD, Nadal-Jimenez, Pol ORCID: 0000-0002-9883-0920, Teixeira, Luis and Xavier, Karina B
(2020) <i>Erwinia carotovora</i> Quorum Sensing System Regulates HostSpecific Virulence Factors and Development Delay in <i>Drosophila melanogaster</i>. MBIO, 11 (3). e01292-e01220.

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Abstract

Multihost bacteria have to rapidly adapt to drastic environmental changes, relying on a fine integration of multiple stimuli for an optimal genetic response. <i>Erwinia carotovora</i> spp. are phytopathogens that cause soft-rot disease. Strain <i>Ecc15</i> in particular is a model for bacterial oral-route infection in <i>Drosophila melanogaster</i> as it harbors a unique gene, <i>evf</i>, that encodes the <i>Erwinia</i> virulence factor (Evf), which is a major determinant for infection of the <i>D. melanogaster</i> gut. However, the factors involved in the regulation of <i>evf</i> expression are poorly understood. We investigated whether <i>evf</i> could be controlled by quorum sensing as, in the <i>Erwinia</i> genus, quorum sensing regulates pectolytic enzymes, the major virulence factors needed to infect plants. Here, we show that transcription of <i>evf</i> is positively regulated by quorum sensing in <i>Ecc15</i> via acyl-homoserine lactone (AHL) signal synthase ExpI and AHL receptors ExpR1 and ExpR2. We also show that the load of <i>Ecc15</i> in the gut depends upon the quorum sensing-mediated regulation of <i>evf</i> Furthermore, we demonstrate that larvae infected with <i>Ecc15</i> suffer a developmental delay as a direct consequence of the regulation of <i>evf</i> via quorum sensing. Finally, we demonstrate that <i>evf</i> is coexpressed with plant cell wall-degrading enzymes (PCWDE) during plant infection in a quorum sensing-dependent manner. Overall, our results show that <i>Ecc15</i> relies on quorum sensing to control production of both pectolytic enzymes and Evf. This regulation influences the interaction of <i>Ecc15</i> with its two known hosts, indicating that quorum sensing signaling may impact bacterial dissemination via insect vectors that feed on rotting plants.<b>IMPORTANCE</b> Integration of genetic networks allows bacteria to rapidly adapt to changing environments. This is particularly important in bacteria that interact with multiple hosts. <i>Erwinia carotovora</i> is a plant pathogen that uses <i>Drosophila melanogaster</i> as a vector. To interact with these two hosts, <i>Ecc15</i> uses different sets of virulence factors: plant cell wall-degrading enzymes to infect plants and the <i>Erwinia</i> virulence factor (<i>evf</i>) to infect <i>Drosophila</i> Our work shows that, despite the virulence factors being specific for each host, both sets are coactivated by homoserine lactone quorum sensing and by the two-component GacS/A system in infected plants. This regulation is essential for <i>Ecc15</i> loads in the gut of <i>Drosophila</i> and minimizes the developmental delay caused by the bacteria with respect to the insect vector. Our findings provide evidence that coactivation of the host-specific factors in the plant may function as a predictive mechanism to maximize the probability of transit of the bacteria between hosts.

Item Type: Article
Uncontrolled Keywords: Drosophila, Ecc15, homoserine lactones, bacterial infections, hostpathogen interactions, insect development, invertebrate-microbe interactions, quorum sensing
Divisions: Faculty of Health and Life Sciences
Faculty of Health and Life Sciences > Institute of Infection, Veterinary and Ecological Sciences
Depositing User: Symplectic Admin
Date Deposited: 20 May 2021 10:48
Last Modified: 03 Feb 2024 09:06
DOI: 10.1128/mBio.01292-20
Open Access URL: http://doi.org/10.1128/mbio.01292-20
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URI: https://livrepository.liverpool.ac.uk/id/eprint/3123425