The ArcZ small RNA activates SlyA production to control contact-dependent antibacterial killing and diffusible antifungal activity in Dickeya solani
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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.
Importance
To colonize host tissues successfully, bacteria deploy specialized weapons against diverse competitors, including rival bacteria and fungi. How bacteria coordinate distinct competitive systems within a unified regulatory program remains poorly resolved. This study demonstrates that the small RNA ArcZ expands its regulatory range by activating the transcription factor SlyA, rather than targeting downstream effector genes individually. This hierarchical architecture enables a single post-transcriptional checkpoint to control both a diffusible antifungal metabolite and a contact-dependent antibacterial secretion system. Although ArcZ and SlyA are broadly conserved across Enterobacterales , the complementary sequence within the slyA 5′ UTR is restricted to Pectobacteriaceae , suggesting that this regulatory interaction emerged through target-site evolution. These findings provide a model for how the evolution of a non-coding target site can recruit conserved regulatory components into a lineage-specific regulatory circuit.
