Cross‐talk between a regulatory small <scp>RNA</scp>, cyclic‐di‐<scp>GMP</scp> signalling and flagellar regulator <scp>FlhDC</scp> for virulence and bacterial behaviours

Yuan, Xiaochen; Khokhani, Devanshi; Wu, Xiaogang; Yang, Fenghuan; Biener, Gabriel; Koestler, Benjamin J.; Raicu, Valerică; He, Chenyang; Waters, Christopher M.; Sundin, George W.; Tian, Fang; Yang, Ching Hong

doi:10.1111/1462-2920.13029

Cited by 35 publications

(52 citation statements)

References 81 publications

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“…D. dadantii produces Pels to degrade the plant cell wall, and production of this virulence factor is negatively regulated by c-di-GMP (Yi et al, 2010, Yuan et al, 2015). In this study, we propose a unique regulatory model that connects c-di-GMP regulation of bacterial virulence to both the global transcriptional and post-transcriptional regulatory systems in D. dadantii .…”

Section: Discussionmentioning

confidence: 99%

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The diguanylate cyclase GcpA inhibits the production of pectate lyases via the H‐NS protein and RsmB regulatory RNA in Dickeya dadantii

Yuan

Tian

et al. 2018

Molecular Plant Pathology

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Dickeya dadantii 3937 secretes pectate lyases (Pels) to degrade plant cell walls. Previously, we have demonstrated that EGcpB and EcpC function as bis-(3',5')-cyclic dimeric guanosine monophosphate (c-di-GMP)-specific phosphodiesterases (PDEs) to positively regulate Pel production. However, the diguanylate cyclase (DGC) responsible for the synthesis of c-di-GMP and the dichotomous regulation of Pel has remained a mystery. Here, we identified GcpA as the dominant DGC to negatively regulate Pel production by the specific repression of pelD gene expression. Quantitative reverse transcription-polymerase chain reaction (qRT-PCR) assays revealed that the expression levels of histone-like, nucleoid-structuring protein encoding gene hns and post-transcriptional regulator encoding genes rsmA and rsmB were significantly affected by GcpA. Deletion of hns or rsmB in the gcpA site-directed mutant restored its Pel production and pelD expression, demonstrating that H-NS and RsmB contribute to the GcpA-dependent regulation of Pel in D. dadantii. In addition, RsmB expression was subject to positive regulation by H-NS. Thus, we propose a novel pathway consisting of GcpA-H-NS-RsmB-RsmA-pelD that controls Pel production in D. dadantii. Furthermore, we showed that H-NS and RsmB are responsible for the GcpA-dependent regulation of motility and type III secretion system (T3SS) gene expression, respectively. Of the two PDEs involved in the regulation of Pels, only EGcpB regulates pelD expression through the same pathway as GcpA.

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Section: Discussionmentioning

confidence: 99%

“…The local leaf maceration assay was performed using the leaves of Chinese cabbage ( B. campestris ) as described (Yuan et al, 2015). In brief, 10 µl of bacterial suspension at 10 7 CFU ml −1 were inoculated into the wounds punched with a sterile pipette on the leaves.…”

Section: Methodsmentioning

confidence: 99%

The diguanylate cyclase GcpA inhibits the production of pectate lyases via the H‐NS protein and RsmB regulatory RNA in Dickeya dadantii

Yuan

Tian

et al. 2018

Molecular Plant Pathology

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“…These RNAs were found to play a role at the posttranscriptional level, being involved in the regulation of diverse physiological processes, such as stress responses, virulence, motility, biofilm formation, quorum sensing, and metabolic control (5)(6)(7)(8)(9)(10)(11)(12)(13)(14). In addition to cis-encoded antisense RNAs, many transencoded RNAs exert their regulatory roles through base pairing with the complementary mRNA target, which involves the chaperone protein Hfq to mediate the sRNA-mRNA interaction (4,14,15).…”

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confidence: 99%

The novel regulatory ncRNA, NfiS, optimizes nitrogen fixation via base pairing with the nitrogenase gene nifK mRNA in Pseudomonas stutzeri A1501

Zhan

Yan

Deng

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

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Unlike most Pseudomonas, the root-associated bacterium Pseudomonas stutzeri A1501 fixes nitrogen after the horizontal acquisition of a nitrogen-fixing (nif) island. A genome-wide search for small noncoding RNAs (ncRNAs) in P. stutzeri A1501 identified the novel P. stutzeri-specific ncRNA NfiS in the core genome, whose synthesis was significantly induced under nitrogen fixation or sorbitol stress conditions. The expression of NfiS was RNA chaperone Hfqdependent and activated by the sigma factor RpoN/global nitrogen activator NtrC/nif-specific activator NifA regulatory cascade. The nfiSdeficient mutant displayed reduced nitrogenase activity, as well as increased sensitivity to multiple stresses, such as osmotic and oxidative stresses. Secondary structure prediction and complementation studies confirmed that a stem-loop structure was essential for NfiS to regulate the nitrogenase gene nifK mRNA synthesis and thus nitrogenase activity. Microscale thermophoresis and physiological analysis showed that NfiS directly pairs with nifK mRNA and ultimately enhances nitrogenase activity by increasing the translation efficiency and the half-life of nifK mRNA. Our data also suggest structural and functional divergence of NfiS evolution in diazotrophic and nondiazotrophic backgrounds. It is proposed that NfiS was recruited by nifK mRNA as a novel regulator to integrate the horizontally acquired nif island into host global networks.nitrogen fixation | Pseudomonas stutzeri | regulatory ncRNA | NfiS | nifK mRNA

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“…As, our results (Fig. B and C) showed that Hfq controls T3SS and Pel through additional pathways independent of PecT, and c‐di‐GMP negatively regulates T3SS, Pel and swimming motility in D. dadantii (Yi et al ., ; Yuan et al ., ; Yuan et al ., ), we further assessed whether Hfq controls T3SS and Pel through c‐di‐GMP signalling. We first compared the intracellular c‐di‐GMP levels between wild‐type and Δ hfq using ultra performance liquid chromatography coupled with tandem mass spectrometry (UPLC‐MS–MS).…”

Section: Resultsmentioning

confidence: 99%

A feed‐forward signalling circuit controls bacterial virulence through linking cyclic di‐GMP and two mechanistically distinct sRNAs, ArcZ and RsmB

Yuan

Zeng

Khokhani

et al. 2019

Environmental Microbiology

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Summary Dickeya dadantii is a plant pathogen that causes soft rot disease on vegetable and potato crops. To successfully cause infection, this pathogen needs to coordinately modulate the expression of genes encoding several virulence determinants, including plant cell wall degrading enzymes (PCWDEs), type III secretion system (T3SS) and flagellar motility. Here, we uncover a novel feed‐forward signalling circuit for controlling virulence. Global RNA chaperone Hfq interacts with an Hfq‐dependent sRNA ArcZ and represses the translation of pecT, encoding a LysR‐type transcriptional regulator. We demonstrate that the ability of ArcZ to be processed to a 50 nt 3′‐ end fragment is essential for its regulation of pecT. PecT down‐regulates PCWDE and the T3SS by repressing the expression of a global post‐transcriptional regulator‐ (RsmA‐) associated sRNA encoding gene rsmB. In addition, we show that the protein levels of two cyclic di‐GMP (c‐di‐GMP) diguanylate cyclases (DGCs), GcpA and GcpL, are repressed by Hfq. Further studies show that both DGCs are essential for the Hfq‐mediated post‐transcriptional regulation on RsmB. Overall, our report provides new insights into the interplays between ubiquitous signalling transduction systems that were most studied independently and sheds light on multitiered regulatory mechanisms for a precise disease regulation in bacteria.

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Cross‐talk between a regulatory small RNA, cyclic‐di‐GMP signalling and flagellar regulator FlhDC for virulence and bacterial behaviours

Cited by 35 publications

References 81 publications

The diguanylate cyclase GcpA inhibits the production of pectate lyases via the H‐NS protein and RsmB regulatory RNA in Dickeya dadantii

The diguanylate cyclase GcpA inhibits the production of pectate lyases via the H‐NS protein and RsmB regulatory RNA in Dickeya dadantii

The novel regulatory ncRNA, NfiS, optimizes nitrogen fixation via base pairing with the nitrogenase gene nifK mRNA in Pseudomonas stutzeri A1501

A feed‐forward signalling circuit controls bacterial virulence through linking cyclic di‐GMP and two mechanistically distinct sRNAs, ArcZ and RsmB

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