Insights into the distinct cooperation between the transcription factor Clp and LeDSF signaling in the regulation of antifungal factors in Lysobacter enzymogenes OH11

Xu, Gaoge; Shi, Xiaofeng; Wang, Ruping; Xu, Huiyong; Du, Liangcheng; Chou, Seemay; Liu, Hongxia; Liu, Youzhou; Qian, Guoliang; Liu, Fengquan

doi:10.1016/j.biocontrol.2016.08.006

Cited by 6 publications

(7 citation statements)

References 33 publications

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“…In marked contrast to the effect of LesR on the Clp levels, inactivation of DSF signaling did not seem to alter the Clp protein level (Additional file 1 : Figure S1). These results, along with our recent report [ 17 ], suggest that although Clp acts as a downstream regulator in both the DSF and LesR regulatory pathways, each pathway appears to use different Clp-dependent mechanism(s) to regulate HSAF biosynthesis in L. enzymogenes .…”

Section: Discussionsupporting

confidence: 76%

“…Recently, a new DSF family signaling molecule, Le DSF3 (13-methyltetradecanoic acid), was shown to modulate HSAF biosynthesis via the conserved RpfC/RpfG two-component system and the global regulator Clp in L. enzymogenes [ 2 , 16 ]. These results strongly suggest that the regulator Clp serves as a downstream component of DSF signaling and controls HSAF biosynthesis in L. enzymogenes , which was recently confirmed by our laboratory and collaborators [ 16 , 17 ]. However, Clp also controls other vital physiological functions, such as cell aggregation in a DSF-independent manner in L. enzymogenes , since the disruption of DSF signaling did not change cell adherence/aggregation, as shown in the clp mutant [ 2 , 14 ].…”

Section: Introductionsupporting

confidence: 79%

“…In the present study, we provide the first report that Clp serves as a downstream factor of the LesR regulatory pathway to control HSAF biosynthesis and cell aggregation in L. enzymogenes , in addition to the characterized DSF signaling pathway [ 6 , 17 ]. This knowledge adds new insights into the complex regulatory pathways that involve the global regulator Clp in bacteria.…”

Section: Discussionmentioning

confidence: 99%

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LesR is a novel upstream regulator that controls downstream Clp expression to modulate antibiotic HSAF biosynthesis and cell aggregation in Lysobacter enzymogenes OH11

Wang

Zhao

et al. 2017

Microb Cell Fact

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BackgroundHeat-stable antifungal factor (HSAF) is a polycyclic tetramate macrolactam secondary metabolite that exhibits broad-spectrum inhibitory activities against filamentous fungal pathogens. The native yield of this chemical is low. It is also a great challenge to synthesize HSAF artificially, due to its complex structure. Understanding the regulatory mechanism underlying HSAF biosynthesis could provide genetic basis for engineering high HSAF-producing strain. The transcription factor Clp is a global regulator that controls bacterial pathogenicity and the expression of one hundred related genes in the phytopathogenic bacterium Xanthomonas campestris pv. campestris (Xcc). Diffusible signal factor (DSF) chemical signaling is the only well-characterized upstream regulatory pathway that involves downstream Clp regulation in Xcc. Such a regulatory hierarchy between DSF signaling and Clp is also conserved in the Gram-negative biological control agent Lysobacter enzymogenes, where the DSF signaling system controls antifungal antibiotic HSAF biosynthesis via Clp.ResultsHere, using LLysobacter enzymogenes OH11 as a working organism, we examined a novel upstream regulator, LesR, a LuxR solo that controls Clp expression to modulate HSAF biosynthesis as well as cell aggregation. We found that the overexpression of lesR in strain OH11 almost entirely shut down HSAF production and accelerated cell aggregation. These changed phenotypes could be rescued by the introduction of plasmid-borne clp in the lesR overexpression background. Consistent with findings, we further found that overexpression of lesR led to a decrease in the Clp level.ConclusionsThese results collectively have shown that LesR could exert its function, i.e., HSAF biosynthesis, via downstream Clp. These findings were subsequently validated by a comparative transcriptome analysis, where the regulatory action of LesR was found to largely overlap with that of Clp. Therefore, in addition to the well-known DSF signaling system, the present study reveals that LesR functions as a new upstream regulatory factor of Clp in L. enzymogenes. The key factor was important for the production of HSAF. The strains with high HSAF yield can presumably be constructed by deletion of the negative regulators or overexpression of the positive regulators by genetic engineering.Electronic supplementary materialThe online version of this article (10.1186/s12934-017-0818-2) contains supplementary material, which is available to authorized users.

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Section: Discussionsupporting

confidence: 76%

Section: Introductionsupporting

confidence: 79%

Section: Discussionmentioning

confidence: 99%

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LesR is a novel upstream regulator that controls downstream Clp expression to modulate antibiotic HSAF biosynthesis and cell aggregation in Lysobacter enzymogenes OH11

Wang

Zhao

et al. 2017

Microb Cell Fact

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“…The possible cross‐talk between Clp regulation and the DSF signalling system was further investigated in L. enzymogenes OH11 by comparing the behaviour of a mutant derivative knocked out in both clp and rpf with the behaviour of mutant derivatives knocked out only in clp or rpf (Xu et al . ). The results showed that production of extracellular lytic enzymes (chitinases and proteases) and twitching motility were controlled by Clp in a DSF‐independent manner.…”

Section: The Regulatory Network In Lysobacter Enzymogenesmentioning

confidence: 97%

“…However, more studies are needed to understand how the DSF signalling system may regulate HSAF biosynthesis through activation of the Clp regulation system (Xu et al . ).…”

Section: The Regulatory Network In Lysobacter Enzymogenesmentioning

confidence: 97%

The impact of the omics era on the knowledge and use ofLysobacterspecies to control phytopathogenic micro-organisms

2017

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Omics technologies have had a tremendous impact on underinvestigated genera of plant disease biocontrol agents such as Lysobacter. Strong evidence of the association between Lysobacter spp. and the rhizosphere has been obtained through culture-independent methods, which has also contributed towards highlighting the relationship between Lysobacter abundance and soil suppressiveness. It is conceivable that the role played by Lysobacter spp. in soil suppressiveness is related to their ability to produce an impressive array of lytic enzymes and antibiotics. Indeed, genomics has revealed that biocontrol Lysobacter strains share a vast number of genes involved in antagonism activities, and the molecular pathways underlying how Lysobacter spp. interact with the environment and other micro-organisms have been depicted through transcriptomic analysis. Furthermore, omics technologies shed light on the regulatory pathways governing cell motility and the biosynthesis of antibiotics. Overall, the results achieved so far through omics technologies confirm that the genus Lysobacter is a valuable source of novel biocontrol agents, paving the way for studies aimed at making their application in field conditions more reliable.

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Diguanylate Cyclase and Phosphodiesterase Interact To Maintain the Specificity of Cyclic di-GMP Signaling in the Regulation of Antibiotic Synthesis in Lysobacter enzymogenes

Zhou

Qian

et al. 2022

Appl Environ Microbiol

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Cyclic dimeric GMP (c-di-GMP) is a universal second messenger in bacteria. The large number of c-di-GMP-related diguanylate cyclases (DGCs), phosphodiesterases (PDEs) and effectors are responsible for the complexity and dynamics of c-di-GMP signaling. Some of these components deploy various methods to avoid undesired crosstalk to maintain signaling specificity. Synthesis of the antibiotic HSAF ( H eat S table A ntifungal F actor) in Lysobacter enzymogenes is regulated by a specific c-di-GMP signaling pathway that includes a PDE LchP and a c-di-GMP effector Clp (also a transcriptional regulator). In the present study, from among 19 DGCs, we identified a diguanylate cyclase, LchD, which participates in this pathway. Subsequent investigation indicates that LchD and LchP physically interact and that the catalytic center of LchD is required for both the formation of the LchD-LchP complex and HSAF production. All the detected phenotypes support that LchD and LchP dispaly local c-di-GMP signaling to regulate HSAF biosynthesis. Although direct evidence is lacking, our investigation, which shows that the interaction between a DGC and a PDE maintains the specificity of c-di-GMP signaling, suggests the possibility of the existence of local c-di-GMP pools in bacteria. Importance Cyclic dimeric GMP (c-di-GMP) is a universal second messenger in bacteria. Signaling of c-di-GMP is complex and dynamic, and it is mediated by a large number of components, including c-di-GMP synthases (diguanylate cyclases. DGCs), c-di-GMP degrading enzymes (phosphodiesterases, PDEs), and c-di-GMP effectors. These components deploy various methods to avoid undesired crosstalk to maintain signaling specificity. In the present study, we identified a DGC that interacted with a PDE to specifically regulate antibiotic biosynthesis in L. enzymogenes . We provide direct evidence to show that the DGC and PDE form a complex, and also indirect evidence to argue that they may balance a local c-di-GMP pool to control the antibiotic production. The results represent an important finding regarding the mechanism of a pair of DGC and PDE to control the expression of specific c-di-GMP signaling pathways.

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Insights into the distinct cooperation between the transcription factor Clp and LeDSF signaling in the regulation of antifungal factors in Lysobacter enzymogenes OH11

Cited by 6 publications

References 33 publications

LesR is a novel upstream regulator that controls downstream Clp expression to modulate antibiotic HSAF biosynthesis and cell aggregation in Lysobacter enzymogenes OH11

LesR is a novel upstream regulator that controls downstream Clp expression to modulate antibiotic HSAF biosynthesis and cell aggregation in Lysobacter enzymogenes OH11

The impact of the omics era on the knowledge and use ofLysobacterspecies to control phytopathogenic micro-organisms

Diguanylate Cyclase and Phosphodiesterase Interact To Maintain the Specificity of Cyclic di-GMP Signaling in the Regulation of Antibiotic Synthesis in Lysobacter enzymogenes

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