Differential regulation of phenazine biosynthesis by RpeA and RpeB in Pseudomonas chlororaphis 30-84

Wang, Dongping; Yu, Jae Hyeon; Pierson, Leland S.; Pierson, Elizabeth A.

doi:10.1099/mic.0.059352-0

Cited by 31 publications

(82 citation statements)

References 42 publications

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“…Electrocompetent cells were prepared and electroporation was performed as described previously [16]. Transconjugants and transformants were selected on LB agar supplemented with appropriate antibiotics.…”

Section: Triparental Conjugation and Electroporationmentioning

confidence: 99%

“…RpeA is a putative sensor kinase shown previously to impact phenazine operon expression in response to medium conditions, suggesting that it may function in detecting the metabolic state or growth rate of cells [21]. RpeB is a response regulator that positively regulates the transcription of pip; however, the mechanism by which RpeB influences pip expression is unknown [16]. Additionally, it was proposed that RpoS may regulate Pip in response to nutrient conditions, since constitutive expression or mutation of rpoS can alter pip expression and phenazine production under different medium conditions [16,18,22].…”

Section: Introductionmentioning

confidence: 99%

“…Previous studies with P. chlororaphis 30-84 established that a hierarchical network of genes regulates the PhzR/PhzI QS system that controls the phenazine biosynthetic operon [16,17]. This includes regulation by the transcriptional regulator Pip, the two-component signal transduction system RpeA/ RpeB, the stationary sigma factor RpoS and the Gac/Rsm system [16][17][18][19][20].…”

Section: Introductionmentioning

confidence: 99%

“…This includes regulation by the transcriptional regulator Pip, the two-component signal transduction system RpeA/ RpeB, the stationary sigma factor RpoS and the Gac/Rsm system [16][17][18][19][20]. Pip is an important positive regulator of QS in P. chlororaphis 30-84 and PCL1391 [16,18]. In P. chlororaphis 30-84, the RpeA/RpeB two-component system is required for pip gene expression.…”

Section: Introductionmentioning

confidence: 99%

“…RpeB is a response regulator that positively regulates the transcription of pip; however, the mechanism by which RpeB influences pip expression is unknown [16]. Additionally, it was proposed that RpoS may regulate Pip in response to nutrient conditions, since constitutive expression or mutation of rpoS can alter pip expression and phenazine production under different medium conditions [16,18,22]. Moreover, RpoS regulation of phenazine production is plausible since phenazine production is correlated with the expression of RpoS-regulated genes important for oxidative stress response [9,23].…”

Section: Introductionmentioning

confidence: 99%

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Disruption of MiaA provides insights into the regulation of phenazine biosynthesis under suboptimal growth conditions in Pseudomonas chlororaphis 30-84

Wang

Pierson

et al. 2017

Microbiology

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Many products of secondary metabolism are activated by quorum sensing (QS), yet even at cell densities sufficient for QS, their production may be repressed under suboptimal growth conditions via mechanisms that still require elucidation. For many beneficial plant-associated bacteria, secondary metabolites such as phenazines are important for their competitive survival and plant-protective activities. Previous work established that phenazine biosynthesis in Pseudomonas chlororaphis 30-84 is regulated by the PhzR/PhzI QS system, which in turn is regulated by transcriptional regulator Pip, two-component system RpeA/RpeB and stationary phase/stress sigma factor RpoS. Disruption of MiaA, a tRNA modification enzyme, altered primary metabolism and growth leading to widespread effects on secondary metabolism, including reduced phenazine production and oxidative stress tolerance. Thus, the miaA mutant provided the opportunity to examine the regulation of phenazine production in response to altered metabolism and growth or stress tolerance. Despite the importance of MiaA for translation efficiency, the most significant effect of miaA disruption on phenazine production was the reduction in the transcription of phzR, phzI and pip, whereas neither the transcription nor translation of RpeB, a transcriptional regulator of pip, was affected. Constitutive expression of rpeB or pip in the miaA mutant completely restored phenazine production, but it resulted in further growth impairment. Constitutive expression of RpoS alleviated sensitivity to oxidative stress resulting from RpoS translation inefficiency in the miaA mutant, but it did not restore phenazine production. Our results support the model that cells curtail phenazine biosynthesis under suboptimal growth conditions via RpeB/Pip-mediated regulation of QS.

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Section: Triparental Conjugation and Electroporationmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

See 3 more Smart Citations

Disruption of MiaA provides insights into the regulation of phenazine biosynthesis under suboptimal growth conditions in Pseudomonas chlororaphis 30-84

Wang

Pierson

et al. 2017

Microbiology

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Roles of the Gac‐Rsm pathway in the regulation of phenazine biosynthesis in Pseudomonas chlororaphis 30‐84

et al. 2013

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The GacS/GacA two-component regulatory system activates the production of secondary metabolites including phenazines crucial for biological control activity in Pseudomonas chlororaphis 30-84. To better understand the role of the Gac system on phenazine regulation, transcriptomic analyses were conducted by comparing the wild-type strain to a gacA mutant. RNA-seq analysis identified 771 genes under GacA control, including many novel genes. Consistent with previous findings, phenazine biosynthetic genes were significantly downregulated in a gacA mutant. The transcript abundances of phenazine regulatory genes such as phzI, phzR, iopA, iopB, rpoS, and pip also were reduced. Moreover, the transcript abundance of three noncoding RNAs (ncRNAs) including rsmX, rsmY, and rsmZ was significantly decreased by gacA mutation consistent with the presence of consensus GacA-binding sites associated with their promoters. Our results also demonstrated that constitutive expression of rsmZ from a non-gac regulated promoter resulted in complete restoration of N-acyl-homoserine lactone (AHL) and phenazine production as well as the expression of other gac-dependent secondary metabolites in gac mutants. The role of RsmA and RsmE in phenazine production also was investigated. Overexpression of rsmE, but not rsmA, resulted in decreased AHL and phenazine production in P. chlororaphis, and only a mutation in rsmE bypassed the requirement for GacA in phenazine gene expression. In contrast, constitutive expression of the phzI/phzR quorum sensing system did not rescue phenazine production in the gacA mutant, indicating the direct posttranscriptional control by Gac on the phenazine biosynthetic genes. On the basis of these results, we propose a model to illustrate the hierarchic role of phenazine regulators modulated by Gac in the control of phenazine production. The transcriptomic analysis also was used to identify additional genes regulated by GacA that may contribute to the biological control capability of strain 30-84.

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Regulation of Phenazine Biosynthesis

Sakhtah

Price-Whelan

Dietrich

2013

Microbial Phenazines

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Microbiologists have historically been struck by both the beautiful pigmentation of phenazine-producing cultures and the high degree of variability in phenazine production among isolates, conditions, and even repeat experiments. Motivated by an interest in controlling phenazine biosynthesis, they have identified many of the factors that affect the regulation of this process. Phenazine production is controlled by complex regulatory networks. The variability of phenazine production can be explained in part by the effects of environmental conditions on these networks and by strain-specific differences in these networks. In this chapter, we describe the components of a common regulatory cascade that is represented in many phenazine-producing pseudomonads. Membrane sensor proteins and two component sensors control the activity of downstream regulators such as quorum sensing systems and RNA-binding proteins and small RNAs; these cytoplasmic regulators then control the production of phenazine biosynthetic proteins. We highlight examples from specific strains and cases where the mechanistic links may vary among them. We also discuss environmental parameters that have been shown to affect phenazine biosynthesis and compare their effects in different isolates. Ongoing work will further elaborate the details of the environmental sensing and regulatory responses that control production of these dramatically colored compounds. New findings have the potential to support enhanced application of phenazine-producing strains in agriculture, where they promote crop health, and the treatment of infections in which phenazines contribute to bacterial pathogenicity.

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Differential regulation of phenazine biosynthesis by RpeA and RpeB in Pseudomonas chlororaphis 30-84

Cited by 31 publications

References 42 publications

Disruption of MiaA provides insights into the regulation of phenazine biosynthesis under suboptimal growth conditions in Pseudomonas chlororaphis 30-84

Disruption of MiaA provides insights into the regulation of phenazine biosynthesis under suboptimal growth conditions in Pseudomonas chlororaphis 30-84

Roles of the Gac‐Rsm pathway in the regulation of phenazine biosynthesis in Pseudomonas chlororaphis 30‐84

Regulation of Phenazine Biosynthesis

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