cAMP and c-di-GMP synergistically support biofilm maintenance through the direct interaction of their effectors

Liu, Cong; Sun, Di; Liu, Jiawen; Chen, Ying; Zhou, Xuge; Ru, Yunrui; Zhu, Jingrong; Liu, Weijie

doi:10.1038/s41467-022-29240-5

Cited by 45 publications

(36 citation statements)

References 81 publications

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“…The cytosolic c-di-GMP measurement was performed as previously described [ 21 ]. Briefly, they were grown in 24-well plate, in the presence of 0.02% Citrox BCL, and collected for up to 24 h. Moreover, a co-culture experiment of L. pneumophila SG68703154 with A549 cells and 0.02% Citrox BCL was set up and supernatant bacteria were harvested by centrifugation at 13,000 g after 24 h. Samples were collected for analysis at 3, 9, 15 and 24 h. The centrifugation was performed at 13,000 g for 2 min and at 4 °C.…”

Section: Methodsmentioning

confidence: 99%

The Effect Citrox BCL on Legionella pneumophila Mechanisms of Biofilm Formation, Oxidative Stress and Virulence

Butucel

Balta²,

McCleery

et al. 2022

Antioxidants

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Legionella pneumophila is responsible for causing Legionnaires’ disease and Pontiac fever, also known as legionellosis. The aim of this study was to investigate the mechanistic effect of a mixture of natural antimicrobials (Citrox BCL) in preventing L. pneumophila biofilm formation and reducing its in vitro virulence. The minimum inhibitory concentrations were detected at 0.06%, and the MBC was established at 0.125%. Based on the growth curve profile, the sub-inhibitory concentration of 0.02% was further used to study the mechanistic implications in the absence of a cytotoxic effect on A549 cells. At 24 h post-infection, Citrox BCL reduced (p = 0.005) the intracellular growth of L. pneumophila when the A549 cells or the bacteria were pre-treated with 0.02% Citrox BCL. This result was replicated when Citrox BCL was added during the 24 h infection assay leading to a reduction in intracellular growth (p = 0.003). Herein we show that at the sub-inhibitory concentration of 0.02%, Citrox CBL lowers the ROS levels in infected A549 cells and causes a 45% reduction in L. pneumophila EPS production, a reduction associated with the decline in biofilm formation. Overall, our results corroborate the low c-di-GMP production with the decrease in biofilm formation and low EPS levels. The low EPS levels seemed to be caused by the downregulation of the tatB and tatC gene expressions. Moreover, inhibition of pvcA and pvcB gene expressions, leading to lower siderophore levels, suggests that Citrox BCL reduces the ability of L. pneumophila to sequester iron and reduce biofilm formation through iron starvation.

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Section: Methodsmentioning

confidence: 99%

The Effect Citrox BCL on Legionella pneumophila Mechanisms of Biofilm Formation, Oxidative Stress and Virulence

Butucel

Balta²,

McCleery

et al. 2022

Antioxidants

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“…Liu et al confirmed that nucleotide second messengers (such as cyclic adenosine monophosphate (cAMP) and cyclic diguanylate (c-di-GMP)) play an important role in regulating biofilm maintenance. It has been reported that pathogenic bacteria have evolved strategies to manipulate host cAMP concentrations [ 75 ]. This discovery provided an important direction for new drug design.…”

Section: Strategies Of Targeting Initial Adhesion Stagementioning

confidence: 99%

Targeted Anti-Biofilm Therapy: Dissecting Targets in the Biofilm Life Cycle

Liu

Xie

et al. 2022

Pharmaceuticals

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Biofilm is a crucial virulence factor for microorganisms that causes chronic infection. After biofilm formation, the bacteria present improve drug tolerance and multifactorial defense mechanisms, which impose significant challenges for the use of antimicrobials. This indicates the urgent need for new targeted technologies and emerging therapeutic strategies. In this review, we focus on the current biofilm-targeting strategies and those under development, including targeting persistent cells, quorum quenching, and phage therapy. We emphasize biofilm-targeting technologies that are supported by blocking the biofilm life cycle, providing a theoretical basis for design of targeting technology that disrupts the biofilm and promotes practical application of antibacterial materials.

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“…Most DGCs and PDEs have transmembrane helix structures which can sense various input signals such as oxygen, light, antibiotics (17), and temperature (24) to regulate the level of c-di-GMP. Previous studies (25, 26) have shown that the intracellular level of c-di-GMP can regulate the conversion between the planktonic state and biofilm state of bacteria. In addition, c-di-GMP can regulate the activity of flagella to control the movement ability of bacteria and then regulate bacterial adhesion, and also regulate the synthesis of extracellular polysaccharides and extracellular proteins to promote the formation of biofilm (25).…”

Section: Introductionmentioning

confidence: 97%

The enhanced expression of genes encoding diguanylate cyclases under cold stress contributes to the adhesion and biofilm formation of Shewanella putrefaciens WS13

et al. 2022

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Shewanella putrefaciens is a special spoilage bacterium of seafood during cold storage, which is easy to form biofilm and bring serious hazard to the seafood quality. Life cycle of biofilm starts after bacterial adhesion, which is essential for the formation and development of biofilm. As a ubiquitous second messenger in bacteria, c-di-GMP regulates the conversion between bacterial planktonic state and biofilm state. In this study, the adhesion and biofilm formation of S. putrefaciens WS13 under 4°C were compared to those under 30°C. Atom force microscope and scanning electron microscope were used to study the bacterial adhesion. Biofilm was analyzed by Fourier transform infrared spectroscopy, Bradford assay and phenol-sulfuric acid method. High-performance liquid chromatographic-tandem mass spectrometric and quantitative real-time PCR were applied to study c-di-GMP level and genes encoding diguanylate cyclases in cells, respectively. Results showed that the swarming mobility of S. putrefaciens WS13 was weaker under 4°C, however, the adhesive force under 4°C was 4–5 times higher than that under 30°C. Biofilm biomass, extracellular polysaccharides and extracellular proteins were 2.5 times, 3 times, and 1.6 times more than those under 30°C, respectively, but biofilm composition formed under both temperatures were similar. c-di-GMP level in S. putrefaciens WS13 under 30°C was no more than half of that in the corresponding growth stage under 4°C. Quantitative real-time PCR analysis also showed that the expression of genes encoding diguanylate cyclases were significantly enhanced under 4°C than that under 30°C. S. putrefaciens WS13 adapted to the cold stress by enhancing the expression of genes encoding diguanylate cyclases to promote bacterial adhesion and biofilm formation. This study provides a theoretical foundation for the research on the cold adaptation mechanism of specific spoilage bacteria of seafood based on c-di-GMP, and also provides a new idea to control seafood quality from the perspective of microbial molecular biology.

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cAMP and c-di-GMP synergistically support biofilm maintenance through the direct interaction of their effectors

Cited by 45 publications

References 81 publications

The Effect Citrox BCL on Legionella pneumophila Mechanisms of Biofilm Formation, Oxidative Stress and Virulence

The Effect Citrox BCL on Legionella pneumophila Mechanisms of Biofilm Formation, Oxidative Stress and Virulence

Targeted Anti-Biofilm Therapy: Dissecting Targets in the Biofilm Life Cycle

The enhanced expression of genes encoding diguanylate cyclases under cold stress contributes to the adhesion and biofilm formation of Shewanella putrefaciens WS13

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