Characterization of the multiple molecular mechanisms underlying RsaL control of phenazine‐1‐carboxylic acid biosynthesis in the rhizosphere bacterium <i>Pseudomonas aeruginosa</i> PA1201

Sun, Shuang; Chen, Bin; Jin, Zi-Jing; Zhou, Lian; Fang, Yun-Ling; Thawai, Chitti; Rampioni, Giordano; He, Yanan

doi:10.1111/mmi.13671

Cited by 16 publications

(35 citation statements)

References 69 publications

(122 reference statements)

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“…PYO production has been linked to QS in many reported studies and to date LasR, RhlR, RsaL, PqsE, PqsR and both AQ signal molecules HHQ and PQS have been found to play a role in the control of its production (Whiteley and Greenberg, 2001 ; Gallagher et al, 2002 ; Diggle et al, 2003 ; Schuster et al, 2003 ; Wagner et al, 2003 ; Rampioni et al, 2007 , 2010 ; Farrow et al, 2008 ; Lu et al, 2009 ; Liang et al, 2011 ; Recinos et al, 2012 ; Cabeen, 2014 ; Sun et al, 2017 ). Although QS controls PYO production, the high sequence conservation between the two phenazine producing operons phz1 and phz2 have made analysing their individual expression by DNA hybridization techniques challenging (Schuster et al, 2003 ; Wagner et al, 2003 ; Rampioni et al, 2007 , 2010 ).…”

Section: Introductionmentioning

confidence: 99%

“…The QS repressor RsaL has also been shown to bind to this promoter in an electrophoretic mobility shift assay (EMSA) at the downstream end of the −10 promoter region, thus acting as a repressor of phz1 transcription (Rampioni et al, 2007 ). Moreover, RsaL exerts an indirect negative effect on phz1 transcription by increasing the production of the phz1 repressor protein CdpR (Sun et al, 2017 ).…”

Section: Introductionmentioning

confidence: 99%

“…Less is known about the regulation of the phz2 promoter (P phzA2 ). The intergenic region between qscR and phz2 was probed for RsaL binding by different groups with negative results (Rampioni et al, 2007 ; Sun et al, 2017 ), hence RsaL appears to control P phzA1 but not P phzA2 . Recinos and colleagues found that phz2 transcription is induced by HHQ under anaerobic conditions (Recinos et al, 2012 ).…”

Section: Introductionmentioning

confidence: 99%

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Differential Regulation of the Phenazine Biosynthetic Operons by Quorum Sensing in Pseudomonas aeruginosa PAO1-N

Higgins

Heeb

Rampioni

et al. 2018

Front. Cell. Infect. Microbiol.

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The Pseudomonas aeruginosa quorum sensing (QS) network plays a key role in the adaptation to environmental changes and the control of virulence factor production in this opportunistic human pathogen. Three interlinked QS systems, namely las, rhl, and pqs, are central to the production of pyocyanin, a phenazine virulence factor which is typically used as phenotypic marker for analysing QS. Pyocyanin production in P. aeruginosa is a complex process involving two almost identical operons termed phzA1B1C1D1E1F1G1 (phz1) and phzA2B2C2D2E2F2G2 (phz2), which drive the production of phenazine-1-carboxylic acid (PCA) which is further converted to pyocyanin by two modifying enzymes PhzM and PhzS. Due to the high sequence conservation between the phz1 and phz2 operons (nucleotide identity > 98%), analysis of their individual expression by RNA hybridization, qRT-PCR or transcriptomics is challenging. To overcome this difficulty, we utilized luminescence based promoter fusions of each phenazine operon to measure in planktonic cultures their transcriptional activity in P. aeruginosa PAO1-N genetic backgrounds impaired in different components of the las, rhl, and pqs QS systems, in the presence or absence of different QS signal molecules. Using this approach, we found that all three QS systems play a role in differentially regulating the phz1 and phz2 phenazine operons, thus uncovering a higher level of complexity to the QS regulation of PCA biosynthesis in P. aeruginosa than previously appreciated.ImportanceThe way the P. aeruginosa QS regulatory networks are intertwined creates a challenge when analysing the mechanisms governing specific QS-regulated traits. Multiple QS regulators and signals have been associated with the production of phenazine virulence factors. In this work we designed experiments where we dissected the contribution of specific QS switches using individual mutations and complementation strategies to gain further understanding of the specific roles of these QS elements in controlling expression of the two P. aeruginosa phenazine operons. Using this approach we have teased out which QS regulators have either indirect or direct effects on the regulation of the two phenazine biosynthetic operons. The data obtained highlight the sophistication of the QS cascade in P. aeruginosa and the challenges in analysing the control of phenazine secondary metabolites.

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Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Differential Regulation of the Phenazine Biosynthetic Operons by Quorum Sensing in Pseudomonas aeruginosa PAO1-N

Higgins

Heeb

Rampioni

et al. 2018

Front. Cell. Infect. Microbiol.

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“…Additionally, the QS repressor RsaL has also been shown to directly bind to a lux box, upstream of the −10 region of the phz1 promoter, and acts as a repressor of phz1 transcription . Moreover, by increasing the production of the phz1 repressor protein CdpR, RsaL indirectly exerts a negative effect on phz1 transcription . But the phz2 regulation was less known.…”

Section: Introductionmentioning

confidence: 99%

phz1 contributes much more to phenazine‐1‐carboxylic acid biosynthesis than phz2 in Pseudomonas aeruginosa rpoS mutant

et al. 2019

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Pseudomonas aeruginosa PAO1, a common opportunistic bacterial pathogen, contains two phenazine-biosynthetic operons, phz1 (). Each of two operons can independently encode a set of enzymes involving in the biosynthesis of phenazine-1-carboxylic acid. As a global transcriptional regulator, RpoS mediates a lot of genes involving secondary metabolites biosynthesis in many bacteria. In an other previous study, it was reported that RpoS deficiency caused overproduction of pyocyanin, a derivative of phenazine-1-carboxylic acid in P. aeruginosa PAO1. But it is not known how RpoS mediates the expression of each of two phz operons and modulates phenazine-1-carboxylic acid biosynthesis in detail. In this study, by deleting the rpoS gene in the mutant PNΔphz1 and the mutant PNΔphz2, we found that the phz1 operon contributes much more to phenazine-1-carboxylic acid biosynthesis than the phz2 operon in the absence of RpoS. With the construction of the translational and transcriptional fusion vectors with the truncated lacZ reporter gene, we demonstrated that RpoS negatively regulates the expression of phz1 and positively controls the expression of phz2, and the regulation of phenazine-1-carboxylic acid biosynthesis mediated by RopS occurs at the posttranscriptional level, not at the transcriptional level. Obviously, two copies of phz operons and their differential expression mediated by RpoS might help P. aeruginosa adapt to its diverse environments and establish infection in its hosts. K E Y W O R D S P. aeruginosa PN, phenazine-1-carboxylic acid, phz1, phz2, RpoS

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“…These diseases, which can reduce yields by 75% or more (3)(4)(5), can be controlled by phenazine-1-carboxylic acid (PCA), an antibiotic produced by not only Pseudomonas spp. but also plant-associated bacteria, such as Burkholderia, Pectobacterium, Brevibacterium, Streptomyces, and others (6)(7)(8)(9)(10). In vitro antibacterial activity of PCA against X. oryzae pv.…”

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confidence: 99%

Ankyrin-Like Protein AnkB Interacts with CatB, Affects Catalase Activity, and Enhances Resistance of Xanthomonas oryzae pv. oryzae and Xanthomonas oryzae pv. oryzicola to Phenazine-1-Carboxylic Acid

Pan

et al. 2018

Appl Environ Microbiol

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pv. oryzae, which causes rice bacterial leaf blight, and pv. oryzicola, which causes rice bacterial leaf streak, are important plant-pathogenic bacteria. A member of the adaptor protein family, ankyrin protein, has been investigated largely in humans but rarely in plant-pathogenic bacteria. In this study, a novel ankyrin-like protein, AnkB, was identified in pv. oryzae and pv. oryzicola. The expression of was significantly upregulated when these bacteria were treated with phenazine-1-carboxylic acid (PCA). is located 58 bp downstream of the gene (which encodes a catalase) in both bacteria, and the gene expression of and catalase activity were reduced following deletion in pv. oryzae and pv. oryzicola. Furthermore, we demonstrated that AnkB directly interacts with CatB by glutathione -transferase (GST) pulldown assays. Deletion of increased the sensitivity of pv. oryzae and pv. oryzicola to HO and PCA, decreased bacterial biofilm formation, swimming ability, and exopolysaccharide (EPS) production, and also reduced virulence on rice. Together our results indicate that the ankyrin-like protein AnkB has important and conserved roles in antioxidant systems and pathogenicity in pv. oryzae and pv. oryzicola. This study demonstrates that the ankyrin protein AnkB directly interacts with catalase CatB in pv. oryzae and pv. oryzicola. Ankyrin protein AnkB can affect the gene expression of , catalase activity, and sensitivity to HO In spp., the locations of genes and and the amino acid sequence of AnkB are highly conserved. It is suggested that in prokaryotes, AnkB plays a conserved role in the defense against oxidative stress.

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Characterization of the multiple molecular mechanisms underlying RsaL control of phenazine‐1‐carboxylic acid biosynthesis in the rhizosphere bacterium Pseudomonas aeruginosa PA1201

Cited by 16 publications

References 69 publications

Differential Regulation of the Phenazine Biosynthetic Operons by Quorum Sensing in Pseudomonas aeruginosa PAO1-N

Differential Regulation of the Phenazine Biosynthetic Operons by Quorum Sensing in Pseudomonas aeruginosa PAO1-N

phz1 contributes much more to phenazine‐1‐carboxylic acid biosynthesis than phz2 in Pseudomonas aeruginosa rpoS mutant

Ankyrin-Like Protein AnkB Interacts with CatB, Affects Catalase Activity, and Enhances Resistance of Xanthomonas oryzae pv. oryzae and Xanthomonas oryzae pv. oryzicola to Phenazine-1-Carboxylic Acid

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