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The ArcZ small RNA activates SlyA production to control contact-dependent antibacterial killing and diffusible antifungal activity in Dickeya solani

Quentin DuboisiD, Marcel SprengeriD, Sebastian KrautwurstiD, Agnès RodrigueiD, Kai PapenfortiD, Laetitia AttaiechiD, Erwan GuegueniD

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Abstract

Bacterial phytopathogens deploy diverse antimicrobial systems, including diffusible secondary metabolites and contact-dependent secretion apparatuses, to compete with coinhabiting microorganisms during host colonization. How the production of these distinct weapons is coordinated remains incompletely understood. Here, we identified a two-tier regulatory cascade by which the Hfq-dependent small RNA (sRNA) ArcZ controls both antibacterial and antifungal antagonism in the phytopathogen Dickeya solani. High-throughput RNA interactome analysis (RIL-seq) shows that ArcZ interacts broadly across the transcriptome and directly base-pairs with the 5' untranslated region of the mRNA encoding the MarR-family transcription factor SlyA, activating its translation. SlyA subsequently binds directly to selected promoter regions within the solanimycin biosynthetic cluster (sol) and the type VI secretion system (T6SS) loci and activates their transcription. The ArcZ-SlyA axis is required for solanimycin mediated antifungal activity against Kluyveromyces lactis and for T6SS-dependent killing of the sympatric pathogen Pectobacterium atrosepticum, demonstrating that the D. solani T6SS mediates interbacterial competition. A compensatory base-pairing mutation between ArcZ and slyA restores both competitive phenotypes, establishing this post-transcriptional interaction as a direct upstream determinant. Together, these results reveal an sRNA controlled regulatory axis that coordinates diffusible antifungal and contact-dependent antibacterial activities.

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