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Regulation of Cyclic Lipopeptide Orfamide A Biosynthesis in Pseudomonas protegens by the Gac-Rsm-LuxR Cascade

ABSTRACT: Orfamide A, a lipopeptide produced by Pseudomonas protegens Pf-5, is a key determinant of its biocontrol properties. In this study, we investigated the regulatory interactions among the GacS/A two-component system, small RNAs (sRNAs), repressor proteins, and two LuxR-type transcription factors in orfamide A biosynthesis. We found that GacS/A indirectly regulates orfamide A production by enhancing transcription of three sRNAs (RsmX, RsmY and RsmZ). RsmY and RsmZ synergistically relieve repression by RsmA and RsmE, while RsmX plays a lesser role, likely counteracting only one repressor. LuxR-type transcription factors LuxR1 and LuxR2, which positively regulate orfamide A synthesis, are directly repressed by RsmA and RsmE via binding to their 5′ untranslated regions, linking them to the Gac-Rsm signaling cascade. We further demonstrate that LuxR2 activates luxR1 expression, which in turn facilitates orfamide A production by binding to the promoter of the orfamide A biosynthetic gene cluster. Importantly, we show that this entire regulatory cascade operates in the rhizosphere and directly influences biocontrol efficacy. These findings provide a comprehensive understanding of the Gac-Rsm-LuxR pathway in orfamide A biosynthesis and offer valuable insights for the development of biocontrol agents based on Pseudomonas strains.

ORGANISM(S): Pseudomonas protegens

PROVIDER: GSE325590 | GEO | 2026/04/01

REPOSITORIES: GEO

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Project description:The GacS/GacA two component regulatory system globally activates the production of secondary metabolites including phenazines in Pseudomonas chlororaphis 30-84. To better understand the regulatory role of the Gac system, we conducted RNA-seq analyses to determine the regulon of the response regulator GacA. Transcriptome analyses identified over 700 genes differentially regulated by GacA. Consistent with our previous findings, phenazine biosynthetic genes were significantly down-regulated in a gacA mutant. The expression levels of phenazine regulatory genes such as phzI, phzR, iopA, iopB, rpoS and pip were also decreased. Moreover, the expression of three none-coding RNAs (ncRNAs) including rsmX, rsmY and rsmZ was significantly decreased by gacA mutation consistent with the presence of GacA binding sites in their promoters. Our results also demonstrated that over-expression of rsmZ from a non-gac regulated promoter resulted in the restoration of AHL and phenazine production as well as the expression of other secondary metabolites in gac mutants. The role of RsmA and RsmE in phenazine production was also investigated. Over-expression of rsmE, but not rsmA, resulted in decreased AHL production and phenazine gene expression in P. chlororaphis. Consistently, a mutation in rsmE bypassed the requirement of GacA in phenazine gene expression. On the contrary, constitutive expression of the phzI/phzR quorum sensing system was not able to rescue phenazine production in the gacA mutant indicating the direct impact of Gac system on the transcript stability of phenazine biosynthetic genes. Together, these results indicate that the Gac system regulates phenazine production at multiple levels and exerts its positive effect on AHL and phenazine biosynthesis via RsmZ and RsmE. A model is proposed to illustrate the GacA regulon in P. chlororaphis 30-84. A total of 6 samples were analyzed in AB medium + 2% casamino acids, Pseudomonas chlororaphis wild type strain (3 replicates); Pseudomonas chlororaphis gacA mutant (3 replicates).

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Regulation of Cyclic Lipopeptide Orfamide A Biosynthesis in Pseudomonas protegens by the Gac-Rsm-LuxR Cascade

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