Quorum Sensing Gene LasR Promotes Phage VB_Pae_PLY Infection in Pseudomonas Aeruginosa

Overview

Journal BMC Microbiol

Publisher Biomed Central

Specialty Microbiology

Date 2024 Jun 10

PMID 38858621

Authors

Yan Liu

Zhuocheng Yao

Zhenzhi Mao

Miran Tang

Huanchang Chen

Changrui Qian

Weiliang Zeng

Tieli Zhou

Qing Wu

Affiliations

Soon will be listed here.

Abstract

Background: Quorum sensing (QS) is a cell density-based intercellular communication system that controls virulence gene expression and biofilm formation. In Pseudomonas aeruginosa (P. aeruginosa), the LasR system sits at the top of the QS hierarchy and coordinates the expression of a series of important traits. However, the role of lasR in phage infection remains unclear. This study aims to investigate the role of lasR QS in phage infection.

Methods: The P. aeruginosa phage was isolated from sewage, and its biological characteristics and whole genome were analyzed. The adsorption receptor was identified via a phage adsorption assay. Following lasR gene knockout, the adsorption rate and bactericidal activity of phage were analyzed. Finally, real-time quantitative polymerase chain reaction (RT-qPCR) was conducted to explore how lasR promoting phage infection.

Results: The lytic phage vB_Pae_PLY was isolated and lipopolysaccharide (LPS) was identified as its adsorption receptor. The adsorption rate and bactericidal activity of vB_Pae_PLY were reduced after lasR knockout. RT-qPCR results showed that the expression of galU, a key gene involved in LPS synthesis, was down-regulated, and several genes related to type IV pili (T4P) were also down-regulated in the lasR mutant PaΔlasR.

Conclusions: The study showed that QS lasR may promote phage vB_Pae_PLY infection by involving in the synthesis of LPS and T4P. This study provides an example of QS in promoting phage infection and deepens the understanding of phage-bacteria interactions.

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References

Donlan R . Preventing biofilms of clinically relevant organisms using bacteriophage. Trends Microbiol. 2009; 17(2):66-72. DOI: 10.1016/j.tim.2008.11.002. View

Schroven K, Putzeys L, Swinnen A, Hendrix H, Paeshuyse J, Lavigne R . The phage-encoded protein PIT2 impacts quorum sensing by direct interaction with LasR. iScience. 2023; 26(10):107745. PMC: 10509696. DOI: 10.1016/j.isci.2023.107745. View

Lee J, Zhang L . The hierarchy quorum sensing network in Pseudomonas aeruginosa. Protein Cell. 2014; 6(1):26-41. PMC: 4286720. DOI: 10.1007/s13238-014-0100-x. View

Xuan G, Lin H, Tan L, Zhao G, Wang J . Quorum Sensing Promotes Phage Infection in Pseudomonas aeruginosa PAO1. mBio. 2022; 13(1):e0317421. PMC: 8764535. DOI: 10.1128/mbio.03174-21. View

Li J, Yan B, He B, Li L, Zhou X, Wu N . Development of phage resistance in multidrug-resistant Klebsiella pneumoniae is associated with reduced virulence: a case report of a personalised phage therapy. Clin Microbiol Infect. 2023; 29(12):1601.e1-1601.e7. DOI: 10.1016/j.cmi.2023.08.022. View

Xuan G, Dou Q, Kong J, Lin H, Wang J . Pseudomonas aeruginosa Resists Phage Infection via Eavesdropping on Indole Signaling. Microbiol Spectr. 2023; 11(1):e0391122. PMC: 9927445. DOI: 10.1128/spectrum.03911-22. View

Xuan G, Lin H, Wang J . Expression of a Phage-Encoded Gp21 Protein Protects Pseudomonas aeruginosa against Phage Infection. J Virol. 2022; 96(5):e0176921. PMC: 8906398. DOI: 10.1128/JVI.01769-21. View

Wang J, Wang C, Yu H, Ahator S, Wu X, Lv S . Bacterial quorum-sensing signal IQS induces host cell apoptosis by targeting POT1-p53 signalling pathway. Cell Microbiol. 2019; 21(10):e13076. DOI: 10.1111/cmi.13076. View

Dunne M, Hupfeld M, Klumpp J, Loessner M . Molecular Basis of Bacterial Host Interactions by Gram-Positive Targeting Bacteriophages. Viruses. 2018; 10(8). PMC: 6115969. DOI: 10.3390/v10080397. View

10.

Broniewski J, Chisnall M, Hoyland-Kroghsbo N, Buckling A, Westra E . The effect of Quorum sensing inhibitors on the evolution of CRISPR-based phage immunity in Pseudomonas aeruginosa. ISME J. 2021; 15(8):2465-2473. PMC: 8319334. DOI: 10.1038/s41396-021-00946-6. View

11.

Xuan G, Tan L, Yang Y, Kong J, Lin H, Wang J . Quorum sensing autoinducers AHLs protect Shewanella baltica against phage infection. Int J Food Microbiol. 2023; 403:110304. DOI: 10.1016/j.ijfoodmicro.2023.110304. View

12.

Rather M, Saha D, Bhuyan S, Jha A, Mandal M . Quorum Quenching: A Drug Discovery Approach Against Pseudomonas aeruginosa. Microbiol Res. 2022; 264:127173. DOI: 10.1016/j.micres.2022.127173. View

13.

Labrie S, Samson J, Moineau S . Bacteriophage resistance mechanisms. Nat Rev Microbiol. 2010; 8(5):317-27. DOI: 10.1038/nrmicro2315. View

14.

De Smet J, Hendrix H, Blasdel B, Danis-Wlodarczyk K, Lavigne R . Pseudomonas predators: understanding and exploiting phage-host interactions. Nat Rev Microbiol. 2017; 15(9):517-530. DOI: 10.1038/nrmicro.2017.61. View

15.

Nobrega F, Vlot M, de Jonge P, Dreesens L, Beaumont H, Lavigne R . Targeting mechanisms of tailed bacteriophages. Nat Rev Microbiol. 2018; 16(12):760-773. DOI: 10.1038/s41579-018-0070-8. View

16.

Testa S, Berger S, Piccardi P, Oechslin F, Resch G, Mitri S . Spatial structure affects phage efficacy in infecting dual-strain biofilms of . Commun Biol. 2019; 2:405. PMC: 6828766. DOI: 10.1038/s42003-019-0633-x. View

17.

Grant J, Enns E, Marinier E, Mandal A, Herman E, Chen C . Proksee: in-depth characterization and visualization of bacterial genomes. Nucleic Acids Res. 2023; 51(W1):W484-W492. PMC: 10320063. DOI: 10.1093/nar/gkad326. View

18.

Hoyland-Kroghsbo N, Maerkedahl R, Svenningsen S . A quorum-sensing-induced bacteriophage defense mechanism. mBio. 2013; 4(1):e00362-12. PMC: 3624510. DOI: 10.1128/mBio.00362-12. View

19.

Li P, Lin H, Mi Z, Xing S, Tong Y, Wang J . Screening of Polyvalent Phage-Resistant Strains Based on Phage Receptor Analysis. Front Microbiol. 2019; 10:850. PMC: 6499177. DOI: 10.3389/fmicb.2019.00850. View

20.

Oechslin F, Piccardi P, Mancini S, Gabard J, Moreillon P, Entenza J . Synergistic Interaction Between Phage Therapy and Antibiotics Clears Pseudomonas Aeruginosa Infection in Endocarditis and Reduces Virulence. J Infect Dis. 2016; 215(5):703-712. PMC: 5388299. DOI: 10.1093/infdis/jiw632. View