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Quorum sensing controls persistence, resuscitation, and virulence of Legionella subpopulations in biofilms

  • 1.

    Newton HJ, Ang DK, van Driel IR, Hartland EL. Molecular pathogenesis of infections caused by Legionella pneumophila. Clin Microbiol Rev. 2010;23:274–98.

    CAS  PubMed  PubMed Central  Google Scholar 

  • 2.

    Hilbi H, Hoffmann C, Harrison CF. Legionella spp. outdoors: colonization, communication and persistence. Environ Microbiol Rep. 2011;3:286–96.

    CAS  PubMed  Google Scholar 

  • 3.

    Fields BS. The molecular ecology of Legionella. Trends Microbiol. 1996;4:286–90.

    CAS  PubMed  Google Scholar 

  • 4.

    Greub G, Raoult D. Microorganisms resistant to free-living amoebae. Clin Microbiol Rev. 2004;17:413–33.

    PubMed  PubMed Central  Google Scholar 

  • 5.

    Hoffmann C, Harrison CF, Hilbi H. The natural alternative: protozoa as cellular models for Legionella infection. Cell Microbiol. 2014;16:15–26.

    CAS  PubMed  Google Scholar 

  • 6.

    Boamah DK, Zhou G, Ensminger AW, O’Connor TJ. From many hosts, one accidental pathogen: The diverse protozoan hosts of Legionella. Front Cell Infect Microbiol. 2017;7:477.

    PubMed  PubMed Central  Google Scholar 

  • 7.

    Swart AL, Harrison CF, Eichinger L, Steinert M, Hilbi H. Acanthamoeba and Dictyostelium as cellular models for Legionella infection. Front Cell Infect Microbiol. 2018;8:61.

    PubMed  PubMed Central  Google Scholar 

  • 8.

    Sherwood RK, Roy CR. A Rab-centric perspective of bacterial pathogen-occupied vacuoles. Cell Host Microbe. 2013;14:256–68.

    CAS  PubMed  Google Scholar 

  • 9.

    Asrat S, de Jesus DA, Hempstead AD, Ramabhadran V, Isberg RR. Bacterial pathogen manipulation of host membrane trafficking. Annu Rev Cell Dev Biol. 2014;30:79–109.

    CAS  PubMed  Google Scholar 

  • 10.

    Finsel I, Hilbi H. Formation of a pathogen vacuole according to Legionella pneumophila: how to kill one bird with many stones. Cell Microbiol. 2015;17:935–50.

    CAS  PubMed  Google Scholar 

  • 11.

    Qiu J, Luo ZQ. Legionella and Coxiella effectors: strength in diversity and activity. Nat Rev Microbiol. 2017;15:591–605.

    CAS  PubMed  Google Scholar 

  • 12.

    Personnic N, Bärlocher K, Finsel I, Hilbi H. Subversion of retrograde trafficking by translocated pathogen effectors. Trends Microbiol. 2016;24:450–62.

    CAS  PubMed  Google Scholar 

  • 13.

    Steiner B, Weber S, Hilbi H. Formation of the Legionella-containing vacuole: phosphoinositide conversion, GTPase modulation and ER dynamics. Int J Med Microbiol. 2018;308:49–57.

    CAS  PubMed  Google Scholar 

  • 14.

    Declerck P. Biofilms: the environmental playground of Legionella pneumophila. Environ Microbiol. 2010;12:557–66.

    CAS  PubMed  Google Scholar 

  • 15.

    Abdel-Nour M, Duncan C, Low DE, Guyard C. Biofilms: the stronghold of Legionella pneumophila. Int J Mol Sci. 2013;14:21660–75.

    PubMed  PubMed Central  Google Scholar 

  • 16.

    Pécastaings S, Allombert J, Lajoie B, Doublet P, Roques C, Vianney A. New insights into Legionella pneumophila biofilm regulation by c-di-GMP signaling. Biofouling. 2016;32:935–48.

    PubMed  Google Scholar 

  • 17.

    Hochstrasser R, Hilbi H. Intra-species and inter-kingdom signaling of Legionella pneumophila. Front Microbiol. 2017;8:79.

    PubMed  PubMed Central  Google Scholar 

  • 18.

    Mampel J, Spirig T, Weber SS, Haagensen JAJ, Molin S, Hilbi H. Planktonic replication is essential for biofilm formation by Legionella pneumophila in a complex medium under static and dynamic flow conditions. Appl Environ Microbiol. 2006;72:2885–95.

    CAS  PubMed  PubMed Central  Google Scholar 

  • 19.

    Hindré T, Brüggemann H, Buchrieser C, Héchard Y. Transcriptional profiling of Legionella pneumophila biofilm cells and the influence of iron on biofilm formation. Microbiology. 2008;154:30–41.

    PubMed  Google Scholar 

  • 20.

    Pécastaings S, Berge M, Dubourg KM, Roques C. Sessile Legionella pneumophila is able to grow on surfaces and generate structured monospecies biofilms. Biofouling. 2010;26:809–19.

    PubMed  Google Scholar 

  • 21.

    Wai SN, Mizunoe Y, Yoshida S. How Vibrio cholerae survive during starvation. FEMS Microbiol Lett. 1999;180:123–31.

    CAS  PubMed  Google Scholar 

  • 22.

    Balaban NQ, Merrin J, Chait R, Kowalik L, Leibler S. Bacterial persistence as a phenotypic switch. Science. 2004;305:1622–5.

    CAS  PubMed  Google Scholar 

  • 23.

    Harms A, Maisonneuve E, Gerdes K. Mechanisms of bacterial persistence during stress and antibiotic exposure. Science. 2016;354:aaf4268.

    PubMed  Google Scholar 

  • 24.

    Claudi B, Sprote P, Chirkova A, Personnic N, Zankl J, Schurmann N, et al. Phenotypic variation of Salmonella in host tissues delays eradication by antimicrobial chemotherapy. Cell. 2014;158:722–33.

    CAS  PubMed  Google Scholar 

  • 25.

    Hélaine S, Cheverton AM, Watson KG, Faure LM, Matthews SA, Holden DW. Internalization of Salmonella by macrophages induces formation of nonreplicating persisters. Science. 2014;343:204–8.

    PubMed  PubMed Central  Google Scholar 

  • 26.

    Conlon BP, Rowe SE, Gandt AB, Nuxoll AS, Donegan NP, Zalis EA, et al. Persister formation in Staphylococcus aureus is associated with ATP depletion. Nat Microbiol. 2016;1:16051.

    CAS  PubMed  PubMed Central  Google Scholar 

  • 27.

    Personnic N, Striednig B, Lezan E, Manske C, Welin A, Schmidt A, et al. Quorum sensing modulates the formation of virulent Legionella persisters within infected cells. Nat Commun. 2019;10:5216.

    PubMed  PubMed Central  Google Scholar 

  • 28.

    Molofsky AB, Swanson MS. Differentiate to thrive: lessons from the Legionella pneumophila life cycle. Mol Microbiol. 2004;53:29–40.

    CAS  PubMed  Google Scholar 

  • 29.

    Hammer BK, Swanson MS. Co-ordination of Legionella pneumophila virulence with entry into stationary phase by ppGpp. Mol Microbiol. 1999;33:721–31.

    CAS  PubMed  Google Scholar 

  • 30.

    Dalebroux ZD, Yagi BF, Sahr T, Buchrieser C, Swanson MS. Distinct roles of ppGpp and DksA in Legionella pneumophila differentiation. Mol Microbiol. 2010;76:200–19.

    CAS  PubMed  PubMed Central  Google Scholar 

  • 31.

    Tiaden A, Spirig T, Hilbi H. Bacterial gene regulation by α-hydroxyketone signaling. Trends Microbiol. 2010;18:288–97.

    CAS  PubMed  Google Scholar 

  • 32.

    Personnic N, Striednig B, Hilbi H. Legionella quorum sensing and its role in pathogen-host interactions. Curr Opin Microbiol. 2018;41:29–35.

    CAS  PubMed  Google Scholar 

  • 33.

    Spirig T, Tiaden A, Kiefer P, Buchrieser C, Vorholt JA, Hilbi H. The Legionella autoinducer synthase LqsA produces an α-hydroxyketone signaling molecule. J Biol Chem. 2008;283:18113–23.

    CAS  PubMed  PubMed Central  Google Scholar 

  • 34.

    Tiaden A, Spirig T, Sahr T, Wälti MA, Boucke K, Buchrieser C, et al. The autoinducer synthase LqsA and putative sensor kinase LqsS regulate phagocyte interactions, extracellular filaments and a genomic island of Legionella pneumophila. Environ Microbiol. 2010;12:1243–59.

    CAS  PubMed  Google Scholar 

  • 35.

    Kessler A, Schell U, Sahr T, Tiaden A, Harrison C, Buchrieser C, et al. The Legionella pneumophila orphan sensor kinase LqsT regulates competence and pathogen-host interactions as a component of the LAI-1 circuit. Environ Microbiol. 2013;15:646–62.

    CAS  PubMed  Google Scholar 

  • 36.

    Tiaden A, Spirig T, Weber SS, Brüggemann H, Bosshard R, Buchrieser C, et al. The Legionella pneumophila response regulator LqsR promotes host cell interactions as an element of the virulence regulatory network controlled by RpoS and LetA. Cell Microbiol. 2007;9:2903–20.

    CAS  PubMed  Google Scholar 

  • 37.

    Tiaden A, Spirig T, Carranza P, Brüggemann H, Riedel K, Eberl L, et al. Synergistic contribution of the Legionella pneumophila lqs genes to pathogen-host interactions. J Bacteriol. 2008;190:7532–47.

    CAS  PubMed  PubMed Central  Google Scholar 

  • 38.

    Schell U, Simon S, Sahr T, Hager D, Albers MF, Kessler A, et al. The α-hydroxyketone LAI-1 regulates motility, Lqs-dependent phosphorylation signalling and gene expression of Legionella pneumophila. Mol Microbiol. 2016;99:778–93.

    CAS  PubMed  Google Scholar 

  • 39.

    Hochstrasser R, Hutter CAJ, Arnold FM, Bärlocher K, Seeger MA, Hilbi H. The structure of the Legionella response regulator LqsR reveals amino acids critical for phosphorylation and dimerization. Mol Microbiol. 2020;113:1070–84.

    CAS  PubMed  Google Scholar 

  • 40.

    Hochstrasser R, Kessler A, Sahr T, Simon S, Schell U, Gomez-Valero L, et al. The pleiotropic Legionella transcription factor LvbR links the Lqs and c-di-GMP regulatory networks to control biofilm architecture and virulence. Environ Microbiol. 2019;21:1035–53.

    CAS  PubMed  Google Scholar 

  • 41.

    Hochstrasser R, Hilbi H. Legionella quorum sensing meets cyclic-di-GMP signaling. Curr Opin Microbiol. 2020;55:9–16.

    CAS  PubMed  Google Scholar 

  • 42.

    Simon S, Schell U, Heuer N, Hager D, Albers MF, Matthias J, et al. Inter-kingdom signaling by the Legionella quorum sensing molecule LAI-1 modulates cell migration through an IQGAP1-Cdc42-ARHGEF9-dependent pathway. PLoS Pathog. 2015;11:e1005307.

    PubMed  PubMed Central  Google Scholar 

  • 43.

    Faucher SP, Friedlander G, Livny J, Margalit H, Shuman HA. Legionella pneumophila 6S RNA optimizes intracellular multiplication. Proc Natl Acad Sci USA. 2010;107:7533–8.

    CAS  PubMed  Google Scholar 

  • 44.

    Faucher SP, Shuman HA. Small regulatory RNA and Legionella pneumophila. Front Microbiol. 2011;2:98.

    CAS  PubMed  PubMed Central  Google Scholar 

  • 45.

    Balaban NQ, Hélaine S, Lewis K, Ackermann M, Aldridge B, Andersson DI, et al. Definitions and guidelines for research on antibiotic persistence. Nat Rev Microbiol. 2019;17:441–8.

    CAS  PubMed  PubMed Central  Google Scholar 

  • 46.

    Brauner A, Fridman O, Gefen O, Balaban NQ. Distinguishing between resistance, tolerance and persistence to antibiotic treatment. Nat Rev Microbiol. 2016;14:320–30.

    CAS  PubMed  Google Scholar 

  • 47.

    Personnic N, Striednig B, Hilbi H. Single cell analysis of Legionella and Legionella-infected Acanthamoeba by agarose embedment. Methods Mol Biol. 2019;1921:191–204.

    CAS  PubMed  Google Scholar 

  • 48.

    Byrne B, Swanson MS. Expression of Legionella pneumophila virulence traits in response to growth conditions. Infect Immun. 1998;66:3029–34.

    CAS  PubMed  PubMed Central  Google Scholar 

  • 49.

    Lewis K. Persister cells, dormancy and infectious disease. Nat Rev Microbiol. 2007;5:48–56.

    CAS  PubMed  Google Scholar 

  • 50.

    Lewis K. Multidrug tolerance of biofilms and persister cells. Curr Top Microbiol Immunol. 2008;322:107–31.

    CAS  PubMed  Google Scholar 

  • 51.

    Hall CW, Mah TF. Molecular mechanisms of biofilm-based antibiotic resistance and tolerance in pathogenic bacteria. FEMS Microbiol Rev. 2017;41:276–301.

    CAS  PubMed  Google Scholar 

  • 52.

    Brenzinger S, van der Aart LT, van Wezel GP, Lacroix JM, Glatter T, Briegel A. Structural and proteomic changes in viable but non-culturable Vibrio cholerae. Front Microbiol. 2019;10:793.

    PubMed  PubMed Central  Google Scholar 

  • 53.

    Defraine V, Fauvart M, Michiels J. Fighting bacterial persistence: current and emerging anti-persister strategies and therapeutics. Drug Resist Updates. 2018;38:12–26.

    Google Scholar 

  • 54.

    Wu B, Liang W, Kan B. Growth phase, oxygen, temperature, and starvation affect the development of viable but non-culturable state of Vibrio cholerae. Front Microbiol. 2016;7:404.

    PubMed  PubMed Central  Google Scholar 

  • 55.

    Ackermann M. A functional perspective on phenotypic heterogeneity in microorganisms. Nat Rev Microbiol. 2015;13:497–508.

    CAS  PubMed  Google Scholar 

  • 56.

    Epstein SS. Microbial awakenings. Nature 2009;457:1083.

    CAS  PubMed  Google Scholar 

  • 57.

    Sturm A, Dworkin J. Phenotypic diversity as a mechanism to exit cellular dormancy. Curr Biol. 2015;25:2272–7.

    CAS  PubMed  PubMed Central  Google Scholar 

  • 58.

    Carlson HK, Vance RE, Marletta MA. H-NOX regulation of c-di-GMP metabolism and biofilm formation in Legionella pneumophila. Mol Microbiol. 2010;77:930–42.

    CAS  PubMed  PubMed Central  Google Scholar 

  • 59.

    Loh E, Righetti F, Eichner H, Twittenhoff C, Narberhaus F. RNA thermometers in bacterial pathogens. Microbiol Spectr. 2018;6.

  • 60.

    Terskikh A, Fradkov A, Ermakova G, Zaraisky A, Tan P, Kajava AV, et al. “Fluorescent timer”: protein that changes color with time. Science. 2000;290:1585–8.

    CAS  PubMed  Google Scholar 


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