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Biofouling
The Journal of Bioadhesion and Biofilm Research
Volume 32, 2016 - Issue 8
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Articles

New insights into Legionella pneumophila biofilm regulation by c-di-GMP signaling

, , , , &
Pages 935-948 | Received 14 Feb 2016, Accepted 07 Jul 2016, Published online: 05 Aug 2016

References

  • Abdel-Nour M, Duncan C, Low DE, Guyard C. 2013. Biofilms: the stronghold of Legionella pneumophila. Int J Mol Sci. 14:21660–21675. doi:10.3390/ijms141121660
  • Abel S, Bucher T, Nicollier M, Hug I, Kaever V, Abel Zur Wiesch P, Jenal U. 2013. Bi-modal distribution of the second messenger c-di-GMP controls cell fate and asymmetry during the caulobacter cell cycle. PLOS Genet. 9:e1003744. doi:10.1371/journal.pgen.1003744
  • Ahmad I, Lamprokostopoulou A, Le Guyon S, Streck E, Barthel M, Peters V, Hardt WD, Römling U. 2011. Complex c-di-GMP signaling networks mediate transition between virulence properties and biofilm formation in Salmonella enterica serovar Typhimurium. PLOS ONE. 6:e28351. doi:10.1371/journal.pone.0028351
  • Ahmad I, Wigren E, Le Guyon S, Vekkeli S, Blanka A, El Mouali Y, Anwar N, Chuah ML, Lünsdorf H, Frank R, et al. 2013. The EAL-like protein STM1697 regulates virulence phenotypes, motility and biofilm formation in Salmonella typhimurium. Mol Microbiol. 90:1216–1232. doi:10.1111/mmi.12428
  • Albert-Weissenberger C, Sahr T, Sismeiro O, Hacker J, Heuner K, Buchrieser C. 2010. Control of flagellar gene regulation in Legionella pneumophila and its relation to growth phase. J Bacteriol. 192:446–455. doi:10.1128/JB.00610-09
  • Allombert J, Lazzaroni JC, Baïlo N, Gilbert C, Charpentier X, Doublet P, Vianney A. 2014. Three antagonistic cyclic di-GMP-catabolizing enzymes promote differential Dot/Icm effector delivery and intracellular survival at the early steps of Legionella pneumophila infection. Infect Immun. 82:1222–1233. doi:10.1128/IAI.01077-13
  • Anwar N, Rouf SF, Römling U, Rhen M. 2014. Modulation of biofilm-formation in Salmonella enterica serovar Typhimurium by the periplasmic DsbA/DsbB oxidoreductase system requires the GGDEF-EAL domain protein STM3615. PLOS ONE. 9:e106095. doi:10.1371/journal.pone.0106095
  • Arora DP, Hossain S, Xu Y, Boon EM. 2015. Nitric oxide regulation of bacterial biofilms. Biochemistry. 54:3717–3728. doi:10.1021/bi501476n
  • Arruebarrena Di Palma A, Pereyra CM, Moreno Ramirez L, Xiqui Vázquez ML, Baca BE, Pereyra MA, Lamattina L, Creus CM. 2013. Denitrification-derived nitric oxide modulates biofilm formation in Azospirillum brasilense. FEMS Microbiol Lett. 338:77–85. doi:10.1111/1574-6968.12030
  • Barraud N, Hassett DJ, Hwang SH, Rice SA, Kjelleberg S, Webb JS. 2006. Involvement of nitric oxide in biofilm dispersal of Pseudomonas aeruginosa. J Bacteriol. 188:7344–7353. doi:10.1128/JB.00779-06
  • Barraud N, Kelso MJ, Rice SA, Kjelleberg S. 2015. Nitric oxide: a key mediator of biofilm dispersal with applications in infectious diseases. Curr Pharm Des. 21:31–42.
  • Barraud N, Schleheck D, Klebensberger J, Webb JS, Hassett DJ, Rice SA, Kjelleberg S. 2009. Nitric oxide signaling in Pseudomonas aeruginosa biofilms mediates phosphodiesterase activity, decreased cyclic di-GMP levels, and enhanced dispersal. J Bacteriol. 191:7333–7342. doi:10.1128/JB.00975-09
  • Barraud N, Storey MV, Moore ZP, Webb JS, Rice SA, Kjelleberg S. 2009. Nitric oxide-mediated dispersal in single- and multi-species biofilms of clinically and industrially relevant microorganisms. Microb Biotechnol. 2:370–378. doi:10.1111/j.1751-7915.2009.00098.x
  • Bigot R, Bertaux J, Frere J, Berjeaud JM. 2013. Intra-amoeba multiplication induces chemotaxis and biofilm colonization and formation for Legionella. PLOS ONE. 8:e77875. doi:10.1371/journal.pone.0077875
  • Bogdan C, Röllinghoff M, Diefenbach A. 2000. The role of nitric oxide in innate immunity. Immunol Rev. 173:17–26.
  • Carlson HK, Vance RE, Marletta MA. 2010. H-NOX regulation of c-di-GMP metabolism and biofilm formation in Legionella pneumophila. Mol Microbiol. 77:930–942. doi:10.1111/j.1365-2958.2010.07259.x
  • Chang B, Sugiyama K, Taguri T, Amemura-Maekawa J, Kura F, Watanabe H. 2009. Specific detection of viable Legionella cells by combined use of photoactivated ethidium monoazide and PCR/real-time PCR. Appl Environ Microbiol. 75:147–153. doi:10.1128/AEM.00604-08
  • Chatfield CH, Cianciotto NP. 2013. Culturing, media, and handling of Legionella. Methods Mol Biol. 954:151–162. doi:10.1007/978-1-62703-161-5_7
  • Delgado-Viscogliosi P, Solignac L, Delattre JM. 2009. Viability PCR, a culture-independent method for rapid and selective quantification of viable Legionella pneumophila cells in environmental water samples. Appl Environ Microbiol. 75:3502–3512. doi:10.1128/AEM.02878-08
  • Fang N, Qu S, Yang H, Fang H, Liu L, Zhang Y, Wang L, Han Y, Zhou D, Yang R. 2014. HmsB enhances biofilm formation in Yersinia pestis. Front Microbiol. 5:685. doi:10.3389/fmicb.2014.00685
  • Fields BS, Benson RF, Besser RE. 2002. Legionella and Legionnaires’ disease: 25 years of investigation. Clin Microbiol Rev. 15:506–526.
  • Henares BM, Xu Y, Boon EM. 2013. A nitric oxide-responsive quorum sensing circuit in Vibrio harveyi regulates flagella production and biofilm formation. Int J Mol Sci. 14:16473–16484. doi:10.3390/ijms140816473
  • Hengge R. 2009. Principles of c-di-GMP signalling in bacteria. Nat Rev Microbiol. 7:263–273. doi:10.1038/nrmicro2109
  • Hindré T, Brüggemann H, Buchrieser C, Héchard Y. 2008. Transcriptional profiling of Legionella pneumophila biofilm cells and the influence of iron on biofilm formation. Microbiology. 154:30–41. doi:10.1099/mic.0.2007/008698-0
  • Hobley L, Fung RK, Lambert C, Harris MA, Dabhi JM, King SS, Basford SM, Uchida K, Till R, Ahmad R, et al. 2012. Discrete cyclic di-GMP-dependent control of bacterial predation versus axenic growth in Bdellovibrio bacteriovorus. PLOS Pathog. 8:e1002493. doi:10.1371/journal.ppat.1002493
  • Hunter JL, Severin GB, Koestler BJ, Waters CM. 2014. The Vibrio cholerae diguanylate cyclase VCA0965 has an AGDEF active site and synthesizes cyclic di-GMP. BMC Microbiol. 14:22. doi:10.1186/1471-2180-14-22
  • Jardeleza C, Rao S, Thierry B, Gajjar P, Vreugde S, Prestidge CA, Wormald PJ. 2014. Liposome-encapsulated ISMN: a novel nitric oxide-based therapeutic agent against Staphylococcus aureus biofilms. PLOS ONE. 9:e92117. doi:10.1371/journal.pone.0092117
  • Kozlova EV, Khajanchi BK, Sha J, Chopra AK. 2011. Quorum sensing and c-di-GMP-dependent alterations in gene transcripts and virulence-associated phenotypes in a clinical isolate of Aeromonas hydrophila. Microb Pathog. 50:213–223. doi:10.1016/j.micpath.2011.01.007
  • Krasteva PV, Giglio KM, Sondermann H. 2012. Sensing the messenger: the diverse ways that bacteria signal through c-di-GMP. Protein Sci. 21:929–948. doi:10.1002/pro.2093
  • Levet-Paulo M, Lazzaroni JC, Gilbert C, Atlan D, Doublet P, Vianney A. 2011. The atypical two-component sensor kinase Lpl0330 from Legionella pneumophila controls the bifunctional diguanylate cyclase-phosphodiesterase Lpl0329 to modulate bis-(3'-5')-cyclic dimeric GMP synthesis. J Biol Chem. 286:31136–31144. doi:10.1074/jbc.M111.231340
  • Levi A, Folcher M, Jenal U, Shuman HA. 2011. Cyclic diguanylate signaling proteins control intracellular growth of Legionella pneumophila. mBio. 2:e00316–e00310. doi:10.1128/mBio.00316-10
  • Li B, Chen JQ. 2013. Development of a sensitive and specific qPCR assay in conjunction with propidium monoazide for enhanced detection of live Salmonella spp. in food. BMC Microbiol. 13:273. doi:10.1186/1471-2180-13-273
  • Li Y, Heine S, Entian M, Sauer K, Frankenberg-Dinkel N. 2013. NO-induced biofilm dispersion in Pseudomonas aeruginosa is mediated by an MHYT domain-coupled phosphodiesterase. J Bacteriol. 195:3531–3542. doi:10.1128/JB.01156-12
  • Liu N, Pak T, Boon EM. 2010. Characterization of a diguanylate cyclase from Shewanella woodyi with cyclase and phosphodiesterase activities. Mol Biosyst. 6:1561–1564. doi:10.1039/c002246b
  • Liu N, Xu Y, Hossain S, Huang N, Coursolle D, Gralnick JA, Boon EM. 2012. Nitric oxide regulation of cyclic di-GMP synthesis and hydrolysis in Shewanella woodyi. Biochemistry. 51:2087–2099. doi:10.1021/bi201753f
  • Mampel J, Spirig T, Weber SS, Haagensen JA, Molin S, Hilbi H. 2006. Planktonic replication is essential for biofilm formation by Legionella pneumophila in a complex medium under static and dynamic flow conditions. Appl Environ Microbiol. 72:2885–2895. doi:10.1128/AEM.72.4.2885-2895.2006
  • Marchler-Bauer A, Anderson JB, Chitsaz F, Derbyshire MK, DeWeese-Scott C, Fong JH, Geer LY, Geer RC, Gonzales NR, Gwadz M, et al. 2009a. CDD: specific functional annotation with the Conserved Domain Database. Nucleic Acids Res. 37:D205–D210. doi:10.1093/nar/gkn845
  • Marchler-Bauer A, Anderson JB, Chitsaz F, Derbyshire MK, DeWeese-Scott C, Fong JH, Geer LY, Geer RC, Gonzales NR, Gwadz M, et al. 2009b. CDD: specific functional annotation with the Conserved Domain Database. Nucleic Acids Res. 37:D205–D210. doi:10.1093/nar/gkn845
  • Martínková M, Kitanishi K, Shimizu T. 2013. Heme-based globin-coupled oxygen sensors: linking oxygen binding to functional regulation of diguanylate cyclase, histidine kinase, and methyl-accepting chemotaxis. J Biol Chem. 288:27702–27711. doi:10.1074/jbc.R113.473249
  • Massie JP, Reynolds EL, Koestler BJ, Cong JP, Agostoni M, Waters CM. 2012. Quantification of high-specificity cyclic diguanylate signaling. Proc Natl Acad Sci USA. 109:12746–12751. doi:10.1073/pnas.1115663109
  • Merritt JH, Ha DG, Cowles KN, Lu W, Morales DK, Rabinowitz J, Gitai Z, O’Toole GA. 2010. Specific Control of Pseudomonas aeruginosa surface-associated behaviors by two c-di-GMP diguanylate cyclases. mBio. 1:e00183-10. doi:10.1128/mBio.00183-10
  • Mills E, Pultz IS, Kulasekara HD, Miller SI. 2011. The bacterial second messenger c-di-GMP: mechanisms of signalling. Cell Microbiol. 13:1122–1129. doi:10.1111/j.1462-5822.2011.01619.x
  • Newell PD, Yoshioka S, Hvorecny KL, Monds RD, O’Toole GA. 2011. Systematic analysis of diguanylate cyclases that promote biofilm formation by Pseudomonas fluorescens Pf0-1. J Bacteriol. 193:4685–4698. doi:10.1128/JB.05483-11
  • Österberg S, Åberg A, Herrera Seitz MK, Wolf-Watz M, Shingler V. 2013. Genetic dissection of a motility-associated c-di-GMP signalling protein of Pseudomonas putida. Environ Microbiol Rep. 5:556–565. doi:10.1111/1758-2229.12045
  • Pagnier I, Merchat M, La Scola B. 2009. Potentially pathogenic amoeba-associated microorganisms in cooling towers and their control. Future Microbiol. 4:615–629. doi:10.2217/fmb.09.25
  • Pécastaings S, Bergé M, Dubourg KM, Roques C. 2010. Sessile Legionella pneumophia is able to grow on surfaces and generate structured monospecies biofilms. Biofouling. 26:809–819. doi:10.1080/08927014.2010.520159
  • Plate L, Marletta MA. 2012. Nitric oxide modulates bacterial biofilm formation through a multicomponent cyclic-di-GMP signaling network. Mol Cell. 46:449–460. doi:10.1016/j.molcel.2012.03.023
  • Plate L, Marletta MA. 2013. Nitric oxide-sensing H-NOX proteins govern bacterial communal behavior. Trends Biochem Sci. 38:566–575. doi:10.1016/j.tibs.2013.08.008
  • Povolotsky TL, Hengge R. 2012. “Life-style” control networks in Escherichia coli: signaling by the second messenger c-di-GMP. J Biotechnol. 160:10–16. doi:10.1016/j.jbiotec.2011.12.024
  • Richter AM, Povolotsky TL, Wieler LH, Hengge R. 2014. Cyclic-di-GMP signalling and biofilm-related properties of the Shiga toxin-producing 2011 German outbreak Escherichia coli O104:H4. EMBO Mol Med. 6:1622–1637. doi:10.15252/emmm.201404309
  • Rojas-Hernández S, Rodríguez-Monroy MA, Moreno-Fierros L, Jarillo-Luna A, Carrasco-Yepez M, Miliar-García A, Campos-Rodríguez R. 2007. Nitric oxide production and nitric oxide synthase immunoreactivity in Naegleria fowleri. Parasitol Res. 101:269–274. doi:10.1007/s00436-007-0495-x
  • Römling U, Galperin MY, Gomelsky M. 2013. Cyclic di-GMP: the first 25 years of a universal bacterial second messenger. Microbiol Mol Biol Rev. 77:1–52. doi:10.1128/MMBR.00043-12
  • Seshasayee AS, Fraser GM, Luscombe NM. 2010. Comparative genomics of cyclic-di-GMP signalling in bacteria: post-translational regulation and catalytic activity. Nucleic Acids Res. 38:5970–5981. doi:10.1093/nar/gkq382
  • Shi H, Xu W, Luo Y, Chen L, Liang Z, Zhou X, Huang K. 2011. The effect of various environmental factors on the ethidium monazite and quantitative PCR method to detect viable bacteria. J Appl Microbiol. 111:1194–1204. doi:10.1111/j.1365-2672.2011.05125.x
  • Simm R, Morr M, Kader A, Nimtz M, Römling U. 2004. GGDEF and EAL domains inversely regulate cyclic di-GMP levels and transition from sessility to motility. Mol Microbiol. 53:1123–1134. doi:10.1111/j.1365-2958.2004.04206.x
  • Spurbeck RR, Tarrien RJ, Mobley HL. 2012. Enzymatically active and inactive phosphodiesterases and diguanylate cyclases are involved in regulation of motility or sessility in Escherichia coli CFT073. mBio. 3:e00307–e00312. doi:10.1128/mBio.00307-12
  • Tamayo R, Pratt JT, Camilli A. 2007. Roles of cyclic diguanylate in the regulation of bacterial pathogenesis. Annu Rev Microbiol. 61:131–148. doi:10.1146/annurev.micro.61.080706.093426
  • Tan H, West JA, Ramsay JP, Monson RE, Griffin JL, Toth IK, Salmond GP. 2014. Comprehensive overexpression analysis of cyclic-di-GMP signalling proteins in the phytopathogen Pectobacterium atrosepticum reveals diverse effects on motility and virulence phenotypes. Microbiology. 160:1427–1439. doi:10.1099/mic.0.076828-0
  • Thomas JM, Ashbolt NJ. 2011. Do free-living amoebae in treated drinking water systems present an emerging health risk? Environ Sci Technol. 45:860–869.
  • Tischler AD, Camilli A. 2004. Cyclic diguanylate (c-di-GMP) regulates Vibrio cholerae biofilm formation. Mol Microbiol. 53:857–869. doi:10.1111/j.1365-2958.2004.04155.x
  • Ulrich LE, Zhulin IB. 2010. The MiST2 database: a comprehensive genomics resource on microbial signal transduction. Nucleic Acids Res. 38:D401–D407. doi:10.1093/nar/gkp940
  • Winkler A, Udvarhelyi A, Hartmann E, Reinstein J, Menzel A, Shoeman RL, Schlichting I. 2014. Characterization of elements involved in allosteric light regulation of phosphodiesterase activity by comparison of different functional BlrP1 states. J Mol Biol. 426:853–868. doi:10.1016/j.jmb.2013.11.018
  • Xu J, Kim J, Koestler BJ, Choi JH, Waters CM, Fuqua C. 2013. Genetic analysis of Agrobacterium tumefaciens unipolar polysaccharide production reveals complex integrated control of the motile-to-sessile switch. Mol Microbiol. 89:929–948. doi:10.1111/mmi.12321

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