A crosstalk between c‐di‐GMP and cAMP in regulating transcription of GcsA, a diguanylate cyclase involved in swimming motility in <i>Pseudomonas putida</i>

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

doi:10.1111/1462-2920.14832

Cited by 11 publications

(11 citation statements)

References 56 publications

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“…Our investigation of another target gene, cyaA , reveals the role of c-di-GMP/FleQ in cAMP synthesis regulation, which is in line with the previous findings that high-level c-di-GMP decreased cAMP content in P. aeruginosa and P. putida ( 28 , 29 ). However, the mechanism behind this negative correlation between the 2 second messengers remains unknown.…”

Section: Discussionsupporting

confidence: 90%

“…cyaA , encoding an adenylate cyclase, is responsible for synthesis of another second messenger, cAMP, in P. putida ( 27 ). Both a previous study in P. aeruginosa and our recent study in P. putida revealed that high-level c-di-GMP can decrease the content of cAMP, but their correlation mechanism remains unclear ( 28 , 29 ). In this study, our result showed that c-di-GMP regulated the expression of cyaA in an FleQ-dependent manner.…”

Section: Resultsmentioning

confidence: 87%

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Identification of c-di-GMP/FleQ-Regulated New Target Genes, Including cyaA , Encoding Adenylate Cyclase, in Pseudomonas putida

et al. 2021

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The bacterial second messenger cyclic diguanylate (c-di-GMP) modulates plankton-to-biofilm lifestyle transition of Pseudomonas species through its transcriptional regulatory effector FleQ. FleQ regulates transcription of biofilm- and flagellum-related genes in response to c-di-GMP. Through transcriptomic analysis and FleQ-DNA binding assay, this study identified five new target genes of c-di-GMP/FleQ in P. putida, including PP_0681, PP_0788, PP_4519 (lapE), PP_5222 (cyaA), and PP_5586. Except lapE encoding an outer membrane pore protein and cyaA encoding an adenylate cyclase, the functions of the other three genes encoding hypothetical proteins remain unknown. FleQ and c-di-GMP coordinately inhibit transcription of PP_0788 and cyaA and promote transcription of PP_0681, lapE, and PP_5586. Both in vitro and in vivo assays show that FleQ binds directly to promoters of the five genes. Further analyses confirm that LapE plays a central role of in the secretion of adhesin LapA and that c-di-GMP/FleQ increases lapE transcription, thereby promoting adhesin secretion and biofilm formation. The adenylate cyclase CyaA is responsible for synthesis of another second messenger, cyclic AMP (cAMP). FleQ and c-di-GMP coordinate to decrease the content of cAMP, suggesting that c-di-GMP and FleQ coregulate cAMP by modulating cyaA expression. Overall, this study adds five new members to the c-di-GMP/FleQ-regulated gene family and reveals the role of c-di-GMP/FleQ in LapA secretion and cAMP synthesis regulation in P. putida. IMPORTANCE c-di-GMP/FleQ promotes the plankton-to-biofilm lifestyle transition at the transcriptional level via FleQ in Pseudomonas species. Identification of new target genes directly regulated by c-di-GMP/FleQ helps to broaden the knowledge of c-di-GMP/FleQ-mediated transcriptional regulation. Regulation of lapE by c-di-GMP/FleQ guarantees highly efficient LapA secretion and biofilm formation. The mechanism of negative correlation between c-di-GMP and cAMP in both P. putida and P. aeruginosa remains unknown. Our result concerning transcriptional inhibition of cyaA by c-di-GMP/FleQ reveals the mechanism underlying the decrease of cAMP content by c-di-GMP in P. putida.

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Section: Discussionsupporting

confidence: 90%

Section: Resultsmentioning

confidence: 87%

Identification of c-di-GMP/FleQ-Regulated New Target Genes, Including cyaA , Encoding Adenylate Cyclase, in Pseudomonas putida

et al. 2021

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“…c‐di‐GMP was extracted and quantitated as described previously (Xiao et al ., 2020). Overnight grown P .…”

Section: Methodsmentioning

confidence: 99%

Wsp system oppositely modulates antibacterial activity and biofilm formation via FleQ‐FleN complex in Pseudomonas putida

Nie

Xiao

Song

et al. 2022

Environmental Microbiology

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Type VI secretion systems (T6SS) are specific antibacterial weapons employed by diverse bacteria to protect themselves from competitors. Pseudomonas putida KT2440 possesses a functional T6SS (K1-T6SS) and exhibits antibacterial activity towards a broad range of bacteria. Here we found that the Wsp signal transduction system regulated K1-T6SS expression via synthesizing the second messenger cyclic di-GMP (c-di-GMP), thus mediating antibacterial activity in P. putida. High-level c-di-GMP produced by Wsp system repressed the transcription of K1-T6SS genes in structural operon and vgrG1 operon. Transcriptional regulator FleQ and ATPase FleN functioned as repressors in the Wsp systemmodulated K1-T6SS transcription. However, FleQ and FleN functioned as activators in biofilm formation, and Wsp system promoted biofilm formation largely in a FleQ/FleN-dependent manner. Furthermore, FleQ-FleN complex bound directly to the promoter of K1-T6SS structural operon in vitro, and c-di-GMP promoted the binding. Besides, P. putida biofilm cells showed higher c-di-GMP levels and lower antibacterial activity than planktonic cells. Overall, our findings reveal a mechanism by which Wsp system oppositely modulates antibacterial activity and biofilm formation via FleQ-FleN, and demonstrate the relationship between plankton/biofilm lifestyles and antibacterial activity in P. putida.

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“…More recently, Xiao et al . (2020) showed that Crp P . putida directly represses the expression of gcs A (a novel diguanylate cyclase involved in the repression of swimming motility) in a cAMP‐dependent manner.…”

Section: Introductionmentioning

confidence: 99%

Low CyaA expression and anti‐cooperative binding of cAMP to CRP frames the scope of the cognate regulon of Pseudomonas putida

Arce-Rodríguez

Nikel

Calles

et al. 2021

Environmental Microbiology

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Summary Although the soil bacterium Pseudomonas putida KT2440 bears a bona fide adenylate cyclase gene (cyaA), intracellular concentrations of 3′,5′‐cyclic adenosine monophosphate (cAMP) are barely detectable. By using reporter technology and direct quantification of cAMP under various conditions, we show that such low levels of the molecule stem from the stringent regulation of its synthesis, efflux and degradation. Poor production of cAMP was the result of inefficient translation of cyaA mRNA. Moreover, deletion of the cAMP‐phosphodiesterase pde gene led to intracellular accumulation of the cyclic nucleotide, exposing an additional cause of cAMP drain in vivo. But even such low levels of the signal sustained activation of promoters dependent on the cAMP‐receptor protein (CRP). Genetic and biochemical evidence indicated that the phenomenon ultimately rose from the unusual binding parameters of cAMP to CRP. This included an ultratight cAMP‐CrpP. putida affinity (KD of 45.0 ± 3.4 nM) and an atypical 1:1 effector/dimer stoichiometry that obeyed an infrequent anti‐cooperative binding mechanism. It thus seems that keeping the same regulatory parts and their relational logic but changing the interaction parameters enables genetic devices to take over entirely different domains of the functional landscape.

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A crosstalk between c‐di‐GMP and cAMP in regulating transcription of GcsA, a diguanylate cyclase involved in swimming motility in Pseudomonas putida

Cited by 11 publications

References 56 publications

Identification of c-di-GMP/FleQ-Regulated New Target Genes, Including cyaA , Encoding Adenylate Cyclase, in Pseudomonas putida

Identification of c-di-GMP/FleQ-Regulated New Target Genes, Including cyaA , Encoding Adenylate Cyclase, in Pseudomonas putida

Wsp system oppositely modulates antibacterial activity and biofilm formation via FleQ‐FleN complex in Pseudomonas putida

Low CyaA expression and anti‐cooperative binding of cAMP to CRP frames the scope of the cognate regulon of Pseudomonas putida

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