Cyclic di‐GMP modulates sessile‐motile phenotypes and virulence in <i>Dickeya oryzae</i> via two PilZ domain receptors

Chen, Yu-fan; Lv, Minna; Liang, Zhibin; Liu, Zhiqing; Zhou, Jianuan; Zhang, Lian-Hui

doi:10.1111/mpp.13200

Cited by 9 publications

(7 citation statements)

References 73 publications

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“…In general, c-di-GMP molecules are dependent on downstream receptors to modulate the corresponding phenotype. And YcgR class receptor was mainly responsible for modulation of bacterial motility in EC1 via its PilZ structural domain(42). Considering the above, this section focused on the interaction of the c-di-GMP receptor YcgR with putrescine pathway proteins.…”

Section: Resultsmentioning

confidence: 99%

Cyclic di-GMP interact with putrescine via a PilZ domain receptor YcgR

Gu¹,

Chen²,

Chen³

et al. 2023

Preprint

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The cell motility is one of the key pathogenic factors that contribute to the virulence ofDickeya oryzea,which is a prevalent bacterial pathogen capable of infecting a range of crops and plants. We showed recently that the bacterial second messenger c-di-GMP, and the putrescine-mediated quorum sensing (QS) system, are both involved in the regulation of the bacterial motility inD. oryzeaEC1. In this study, we set to determine whether and how there two signaling mechanisms work together to modulate the bacterial motility. The results showed that the second messenger signaling system interacts with the putrescine QS system via the c-di-GMP receptor YcgR, which could promote the activity of SpeA, the rate-limiting enzyme in the putrescine biosynthesis pathway, thereby increasing the intracellular putrescine levels. However, it was shown that this facilitative effect could be inhibited by c-di-GMP molecules. In addition, we demonstrated the dominance of c-di-GMP over putrescine in the regulation of bacterial motility. The findings from this study provide the first insight into the interaction between c-di-GMP and putrescine in bacteria and provide a valuable reference for the study of intracellular second messenger system and polyamine-mediated quorum sensing system in other bacteria.ImportanceDickea oryzeais a major bacterial pathogen capable of infesting many plants and crops, causing significant economic damage to rice and banana production especially. Bacterial motility is a key pathogenic factor ofD. oryzeato compete for food resources and infect their host species, which is negatively regulated by c-di-GMP and positively regulated by putrescine, respectively. However, the connection between c-di-GMP and putrscine in regulating the motility ofD.oryzeais not understood. Here we revealed the link and the mechanism of interaction between them, showing that c-di-GMP interact with putrescine via a receptor of c-di-GMP. The significance of our research is in providing the first insight into the interaction between c-di-GMP and putrescine and the methods and experimental designs in our study will provide a valuable reference for subsequent studies on the link between c-di-GMP and putrescine in other bacteria and even the regulatory mechanisms of complex bacterial motility networks, respectively.

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Section: Resultsmentioning

confidence: 99%

Cyclic di-GMP interact with putrescine via a PilZ domain receptor YcgR

Gu¹,

Chen²,

Chen³

et al. 2023

Preprint

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“…c‐di‐GMP was measured following a previous study with slight modifications (Chen et al, 2022). Overnight bacterial culture was diluted in 1:100 in 10 ml of MM and strains were grown to OD 600 0.6–0.8 at 28°C, 200 rpm.…”

Section: Methodsmentioning

confidence: 99%

The integration host factor regulates multiple virulence pathways in bacterial pathogen Dickeya zeae MS2

Chen

et al. 2022

Molecular Plant Pathology

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Dickeya zeae is an aggressive bacterial phytopathogen that infects a wide range of host plants. It has been reported that integration host factor (IHF), a nucleoidassociated protein consisting of IHFα and IHFβ subunits, regulates gene expression by influencing nucleoid structure and DNA bending. To define the role of IHF in the pathogenesis of D. zeae MS2, we deleted either and both of the IHF subunit encoding genes ihfA and ihfB, which significantly reduced the production of cell wall-degrading enzymes (CWDEs), an unknown novel phytotoxin and the virulence factor-modulating (VFM) quorum-sensing (QS) signal, cell motility, biofilm formation, and thereafter the infection ability towards both potato slices and banana seedlings. To characterize the regulatory pathways of IHF protein associated with virulence, IHF binding sites (consensus sequence 5′-WATCAANNNNTTR-3′) were predicted and 272 binding sites were found throughout the genome. The expression of 110 tested genes was affected by IHF. Electrophoretic mobility shift assay (EMSA) showed direct interaction of IhfA protein with the promoters of vfmE, speA, pipR, fis, slyA, prtD, hrpL, hecB, hcp, indA, hdaA, flhD, pilT, gcpJ, arcA, arcB, and lysR. This study clarified the contribution of IHF in the pathogenic process of D. zeae by controlling the production of VFM and putrescine QS signals, phytotoxin, and indigoidine, the luxR-solo system, Fis, SlyA, and FlhD transcriptional regulators, and secretion systems from type I to type VI.Characterization of the regulatory networks of IHF in D. zeae provides a target for prevention and control of plant soft rot disease.

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“…c-di-GMP measurement by liquid chromatography-mass spectrometry c-di-GMP was measured following a previous study with slight modifications (Chen et al, 2022). Overnight bacterial culture was 1:50 diluted and grown to OD 600 of 1.0.…”

Section: Biofilm Assaymentioning

confidence: 99%

Genome characterization of a uropathogenic Pseudomonas aeruginosa isolate PA_HN002 with cyclic di-GMP-dependent hyper-biofilm production

Lin

Chen

et al. 2022

Front. Cell. Infect. Microbiol.

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Pseudomonas aeruginosa can cause various types of infections and is one of the most ubiquitous antibiotic-resistant pathogens found in healthcare settings. It is capable of adapting to adverse conditions by transforming its motile lifestyle to a sessile biofilm lifestyle, which induces a steady state of chronic infection. However, mechanisms triggering the lifestyle transition of P. aeruginosa strains with clinical significance are not very clear. In this study, we reported a recently isolated uropathogenic hyper-biofilm producer PA_HN002 and characterized its genome to explore genetic factors that may promote its transition into the biofilm lifestyle. We first showed that high intracellular c-di-GMP content in PA_HN002 gave rise to its attenuated motilities and extraordinary strong biofilm. Reducing the intracellular c-di-GMP content by overexpressing phosphodiesterases (PDEs) such as BifA or W909_14950 converted the biofilm and motility phenotypes. Whole genome sequencing and comprehensive analysis of all the c-di-GMP metabolizing enzymes led to the identification of multiple mutations within PDEs. Gene expression assays further indicated that the shifted expression profile of c-di-GMP metabolizing enzymes in PA_HN002 might mainly contribute to its elevated production of intracellular c-di-GMP and enhanced biofilm formation. Moreover, mobile genetic elements which might interfere the endogenous regulatory network of c-di-GMP metabolism in PA_HN002 were analyzed. This study showed a reprogrammed expression profile of c-di-GMP metabolizing enzymes which may promote the pathoadaption of clinical P. aeruginosa into biofilm producers.

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Cyclic di‐GMP modulates sessile‐motile phenotypes and virulence in Dickeya oryzae via two PilZ domain receptors

Cited by 9 publications

References 73 publications

Cyclic di-GMP interact with putrescine via a PilZ domain receptor YcgR

Cyclic di-GMP interact with putrescine via a PilZ domain receptor YcgR

The integration host factor regulates multiple virulence pathways in bacterial pathogen Dickeya zeae MS2

Genome characterization of a uropathogenic Pseudomonas aeruginosa isolate PA_HN002 with cyclic di-GMP-dependent hyper-biofilm production

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