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AzeR, a transcriptional regulator that responds to azelaic acid in Pseudomonas nitroreducens.

ABSTRACT: Azelaic acid is a dicarboxylic acid that has recently been shown to play a role in plant-bacteria signalling and also occurs naturally in several cereals. Several bacteria have been reported to be able to utilize azelaic acid as a unique source of carbon and energy, including Pseudomonas nitroreducens. In this study, we utilize P. nitroreducens as a model organism to study bacterial degradation of and response to azelaic acid. We report genetic evidence of azelaic acid degradation and the identification of a transcriptional regulator that responds to azelaic acid in P. nitroreducens DSM 9128. Three mutants possessing transposons in genes of an acyl-CoA ligase, an acyl-CoA dehydrogenase and an isocitrate lyase display a deficient ability in growing in azelaic acid. Studies on transcriptional regulation of these genes resulted in the identification of an IclR family repressor that we designated as AzeR, which specifically responds to azelaic acid. A bioinformatics survey reveals that AzeR is confined to a few proteobacterial genera that are likely to be able to degrade and utilize azelaic acid as the sole source of carbon and energy.

SUBMITTER: Bez C

PROVIDER: S-EPMC7398562 | biostudies-literature | 2020 Jan

REPOSITORIES: biostudies-literature

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AzeR, a transcriptional regulator that responds to azelaic acid in Pseudomonas nitroreducens.

Bez Cristina C Javvadi Sree Gowrinadh SG Bertani Iris I Devescovi Giulia G Guarnaccia Corrado C Studholme David J DJ Geller Alexander M AM Levy Asaf A Venturi Vittorio V

Microbiology (Reading, England) 20200101 1

Azelaic acid is a dicarboxylic acid that has recently been shown to play a role in plant-bacteria signalling and also occurs naturally in several cereals. Several bacteria have been reported to be able to utilize azelaic acid as a unique source of carbon and energy, including Pseudomonas nitroreducens. In this study, we utilize P. nitroreducens as a model organism to study bacterial degradation of and response to azelaic acid. We report genetic evidence of azelaic acid degradation ...[more]

PMID: 31621557

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Project description:Diffusible signal factor (DSF) represents a family of widely conserved quorum-sensing (QS) signals which regulate virulence factor production and pathogenicity in numerous Gram-negative bacterial pathogens. We recently reported the identification of a highly potent DSF-quenching bacterial isolate, Pseudomonas nitroreducens HS-18, which contains an operon with four DSF-inducible genes, digABCD, or digA-D, that are responsible for degradation of DSF signals. However, the regulatory mechanisms that govern the digA-D response to DSF induction have not yet been characterized. In this study, we identified a novel transcriptional regulator we designated RdmA (regulator of DSF metabolism) which negatively regulates the expression of digA-D and represses DSF degradation. In addition, we found that a gene cluster located adjacent to rdmA was also negatively regulated by RdmA and played a key role in DSF degradation; this cluster was hence named dmg (DSF metabolism genes). An electrophoretic mobility shift assay and genetic analysis showed that RdmA represses the transcriptional expression of the dmg genes in a direct manner. Further studies demonstrated that DSF acts as an antagonist and binds to RdmA, which abrogates RdmA binding to the target promoter and its suppression on transcriptional expression of the dmg genes. Taken together, the results from this study have unveiled a central regulator and a gene cluster associated with the autoinduction of DSF degradation in P. nitroreducens HS-18, and this will aid in the understanding of the genetic basis and regulatory mechanisms that govern the quorum-quenching activity of this potent biocontrol agent. IMPORTANCE DSF family quorum-sensing (QS) signals play important roles in regulation of bacterial physiology and virulence in a wide range of plant and human bacterial pathogens. Quorum quenching (QQ), which acts by either degrading QS signals or blocking QS communication, has proven to be a potent disease control strategy, but QQ mechanisms that target DSF family signals and associated regulatory mechanisms remain largely unknown. Recently, we identified four autoinduced DSF degradation genes (digABCD) in P. nitroreducens HS-18. By using a combination of transcriptome and genetic analysis, we identified a central regulator that plays a key role in autoinduction of dig expression, as well as a new gene cluster (dmgABCDEFGH) involved in DSF degradation. The significance of our study is in unveiling the autoinduction mechanism that governs DSF signal quorum quenching for the first time, to our knowledge, and in identification of new genes and enzymes responsible for DSF degradation. The findings from this study shed new light on our understanding of the DSF metabolism pathway and the regulatory mechanisms that modulate DSF quorum quenching and will provide useful clues for design and development of a new generation of highly potent QQ biocontrol agents against DSF-mediated bacterial infections.

Dataset Information

AzeR, a transcriptional regulator that responds to azelaic acid in Pseudomonas nitroreducens.

Publications

AzeR, a transcriptional regulator that responds to azelaic acid in <i>Pseudomonas nitroreducens</i>.

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