A natural single nucleotide mutation in the small regulatory RNA ArcZ of Dickeya solani switches off the antimicrobial activities against yeast and bacteria

PLoS Genet. 2023 Apr 27;19(4):e1010725. doi: 10.1371/journal.pgen.1010725. eCollection 2023 Apr.

Abstract

The necrotrophic plant pathogenic bacterium Dickeya solani emerged in the potato agrosystem in Europe. All isolated strains of D. solani contain several large polyketide synthase/non-ribosomal peptide synthetase (PKS/NRPS) gene clusters. Analogy with genes described in other bacteria suggests that the clusters ooc and zms are involved in the production of secondary metabolites of the oocydin and zeamine families, respectively. A third cluster named sol was recently shown to produce an antifungal molecule. In this study, we constructed mutants impaired in each of the three secondary metabolite clusters sol, ooc, and zms to compare first the phenotype of the D. solani wild-type strain D s0432-1 with its associated mutants. We demonstrated the antimicrobial functions of these three PKS/NRPS clusters against bacteria, yeasts or fungi. The cluster sol, conserved in several other Dickeya species, produces a secondary metabolite inhibiting yeasts. Phenotyping and comparative genomics of different D. solani wild-type isolates revealed that the small regulatory RNA ArcZ plays a major role in the control of the clusters sol and zms. A single-point mutation, conserved in some Dickeya wild-type strains, including the D. solani type strain IPO 2222, impairs the ArcZ function by affecting its processing into an active form.

MeSH terms

  • Antimicrobial Peptides* / genetics
  • Antimicrobial Peptides* / pharmacology
  • Ascomycota / drug effects
  • Bacteria / drug effects
  • Dickeya / genetics
  • Dickeya / metabolism
  • Gene Expression Regulation, Bacterial / genetics
  • Genomics
  • Multigene Family* / genetics
  • Point Mutation*
  • Polyketide Synthases / genetics
  • RNA, Bacterial / genetics
  • RNA, Bacterial / metabolism

Substances

  • RNA, Bacterial
  • Polyketide Synthases
  • non-ribosomal peptide synthase
  • Antimicrobial Peptides

Supplementary concepts

  • Dickeya solani

Grants and funding

This work was supported by grants from Agence Nationale de la Recherche to L.A. (Project RNAchap, ANR-17-CE11-0009-01) and to E.G. (Project Tn-Phyto, ANR-19-CE35-0016). E.G was also supported by the FR BioEEnVis, and by annual credits from the University Lyon I and the CNRS at regular basis. T.B. was supported by a PhD grant from the Ministère de l’Enseignement Supérieur, de la Recherche et de l’Innovation. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.