FleN and FleQ play a synergistic role in regulating lapA and bcs operons in Pseudomonas putida KT2440

Nie, Hailing; Xiao, Yujie; Liu, Huizhong; He, Jinzhi; Chen, Wenli; Huang, Qiaoyun

doi:10.1111/1758-2229.12547

Cited by 15 publications

(37 citation statements)

References 39 publications

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“…In P. aeruginosa, FleN acts as an auxiliary element and antagonizes the activator-repressor dual function of FleQ for the regulation of certain genes and operons (Dasgupta et al, 2000;Baraquet et al, 2012). In P. putida, FleN and FleQ also usually play opposite roles, with some exceptions such as their synergistic role in regulating transcription of the bcs biofilm operon and lapA adhesin (Nie et al, 2017).…”

Section: Introductionmentioning

confidence: 99%

The Wsp intermembrane complex mediates metabolic control of the swim‐attach decision of Pseudomonas putida

Hueso-Gil

Calles

2020

Environmental Microbiology

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Summary Pseudomonas putida is a microorganism of biotechnological interest that—similar to many other environmental bacteria—adheres to surfaces and forms biofilms. Although various mechanisms contributing to the swim‐attach decision have been studied in this species, the role of a 7‐gene operon homologous to the wsp cluster of Pseudomonas aeruginosa—which regulates cyclic di‐GMP (cdGMP) levels upon surface contact—remained to be investigated. In this work, the function of the wsp operon of P. putida KT2440 has been characterized through inspection of single and multiple wsp deletion variants, complementation with Pseudomonas aeruginosa's homologues, combined with mutations of regulatory genes fleQ and fleN and removal of the flagellar regulator fglZ. The ability of the resulting strains to form biofilms at 6 and 24 h under three different carbon regimes (citrate, glucose and fructose) revealed that the Wsp complex delivers a similar function to both Pseudomonas species. In P. putida, the key components include WspR, a protein that harbours the domain for producing cdGMP, and WspF, which controls its activity. These results not only contribute to a deeper understanding of the network that regulates the sessile‐planktonic decision of P. putida but also suggest strategies to exogenously control such a lifestyle switch.

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Section: Introductionmentioning

confidence: 99%

The Wsp intermembrane complex mediates metabolic control of the swim‐attach decision of Pseudomonas putida

Hueso-Gil

Calles

2020

Environmental Microbiology

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“…Recent work by our lab and others has also highlighted the importance of FleQ and c-di-GMP in the switch from the planktonic to the sessile lifestyle and vice versa in P . putida [23,25]. Transcription of the flagellar cluster is subjected to a regulatory cascade in which the σ N -dependent activator FleQ is the master regulator, c-di-GMP antagonizes FleQ activation, and the flagellar σ factor FliA directs transcription of late flagellar and chemotaxis genes.…”

Section: Introductionmentioning

confidence: 99%

“…aeruginosa [44], and has recently been shown to play a similar role in the lapA and bcs operons in P . putida [25].…”

Section: Introductionmentioning

confidence: 99%

Transcriptional organization, regulation and functional analysis of flhF and fleN in Pseudomonas putida

et al. 2019

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The Pseudomonas putida flhA-flhF-fleN-fliA cluster encodes a component of the flagellar export gate and three regulatory elements potentially involved in flagellar biogenesis and other functions. Here we show that these four genes form an operon, whose transcription is driven from the upstream PflhA promoter. A second promoter, PflhF, provides additional transcription of the three distal genes. PflhA and PflhF are σN-dependent, activated by the flagellar regulator FleQ, and negatively regulated by FleN. Motility, surface adhesion and colonization defects of a transposon insertion mutant in flhF revealed transcriptional polarity on fleN and fliA, as the former was required for strong surface adhesion and biofilm formation, and the latter was required for flagellar synthesis. On the other hand, FlhF and FleN were necessary to attain proper flagellar location and number for a fully functional flagellar complement. FleN, along with FleQ and the second messenger c-di-GMP differentially regulated transcription of lapA and the bcs operon, encoding a large adhesion protein and cellulose synthase. FleQ positively regulated the PlapA promoter and activation was antagonized by FleN and c-di-GMP. PbcsD was negatively regulated by FleQ and FleN, and repression was antagonized by c-di-GMP. FleN promoted FleQ binding to both PlapA and PbcsD in vitro, while c-di-GMP antagonized interaction with PbcsD and stimulated interaction with PlapA. A single FleQ binding site in PlapA was critical to activation in vivo. Our results suggest that FleQ, FleN and c-di-GMP cooperate to coordinate the regulation of flagellar motility and biofilm development.

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“…In the regulation of flagellar operons, FleQ works along with the alternative σ factor RpoN 2 . It also works together with the anti-activator FleN, another ATPase, by means of direct protein-protein interactions 11–15 . It has also been shown that FleQ can specifically bind the bacterial second messenger cyclic di-guanosine monophosphate (c-di-GMP) 16,17 and the crystal structure of FleQ bound to c-di-GMP has been resolved 18 .…”

Section: Introductionmentioning

confidence: 99%

Genome-wide analysis of the FleQ direct regulon in Pseudomonas fluorescens F113 and Pseudomonas putida KT2440

Blanco-Romero

Redondo‐Nieto

Martínez‐Granero

et al. 2018

Sci Rep

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Bacterial motility plays a crucial role in competitiveness and colonization in the rhizosphere. In this work, Chromatin ImmunoPrecipitation Sequencing (ChIP-seq) analysis has been used to identify genes putatively regulated by the transcriptional regulatory protein FleQ in Pseudomonas fluorescens F113 and Pseudomonas putida KT2440. This protein was previously identified as a master regulator of flagella and biofilm formation in both strains. This work has demonstrated that FleQ from both bacteria are conserved and functionally equivalent for motility regulation. Furthermore, the ChIP-seq analysis has shown that FleQ is a global regulator with the identification of 121 and 103 FleQ putative binding sites in P. fluorescens F113 and P. putida KT2440 respectively. Putative genes regulated by FleQ included, as expected, flagellar and motility-related genes and others involved in adhesion and exopolysaccharide production. Surprisingly, the ChIP-seq analysis also identified iron homeostasis-related genes for which positive regulation was shown by RT-qPCR. The results also showed that FleQ from P. fluorescens F113 shares an important part of its direct regulon with AmrZ, a global regulator also implicated in environmental adaption. Although AmrZ also regulates motility and iron uptake, the overlap occurred mostly with the iron-related genes, since both regulators control a different set of motility-related genes.

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FleN and FleQ play a synergistic role in regulating lapA and bcs operons in Pseudomonas putida KT2440

Cited by 15 publications

References 39 publications

The Wsp intermembrane complex mediates metabolic control of the swim‐attach decision of Pseudomonas putida

The Wsp intermembrane complex mediates metabolic control of the swim‐attach decision of Pseudomonas putida

Transcriptional organization, regulation and functional analysis of flhF and fleN in Pseudomonas putida

Genome-wide analysis of the FleQ direct regulon in Pseudomonas fluorescens F113 and Pseudomonas putida KT2440

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