References

microbe

Проблемы особо опасных инфекций

Problems of Particularly Dangerous Infections

0370-10692658-719X

Russian Research Anti-Plague Institute “Microbe”

10.21055/0370-1069-2019-3-19-25

microbe-1170

Research Article

ОБЗОРЫ

REVIEWS

Биопленка Vibrio cholerae: механизмы, регулирующие образование, и сигналы внешней среды, способствующие ее формированию

Vibrio cholerae Biofilm: Mechanisms, Regulating Formation and Signals of External Environment, Factoring Its Production

Плеханов

Н. А.

Plekhanov

N. A.

410005, Саратов, ул. Университетская, 46.

46, Universitetskaya St., Saratov, 410005.

rusrapi@microbe.ru

Заднова

С. П.

Zadnova

S. P.

410005, Саратов, ул. Университетская, 46.

46, Universitetskaya St., Saratov, 410005.

rusrapi@microbe.ru

Крицкий

А. А.

Kritsky

A. A.

410005, Саратов, ул. Университетская, 46.

46, Universitetskaya St., Saratov, 410005.

rusrapi@microbe.ru

Российский научно-исследовательский противочумный институт «Микроб»РоссияRussian Research Anti-Plague Institute ‘‘Microbe"Russian Federation

2019

12102019

031925

2019

Плеханов Н.А., Заднова С.П., Крицкий А.А.

Plekhanov N.A., Zadnova S.P., Kritsky A.A.

Данная работа распространяется под лицензией Creative Commons Attribution 4.0.

This work is licensed under a Creative Commons Attribution 4.0 License.

https://journal.microbe.ru/jour/article/view/1170

В настоящее время общепризнанным является факт, что способность возбудителя холеры формировать биопленку повышает его выживаемость и сохранение как во внешней среде, так и в макроорганизме. в ассоцииро-ванном состоянии клетки V. cholerae лучше защищены от действия целого ряда стрессовых факторов, более эффективно потребляют питательные вещества и обмениваются генетической информацией. процесс образования биопленки холерным вибрионом изучен достаточно детально. однако, учитывая важную роль данной структуры в жизненном цикле V. cholerae, исследователи, используя современные методы анализа, получают новые данные или уточняют ранее полученные сведения о лежащих в основе этого процесса молекулярных механизмах. при этом особое внимание уделяется изучению регуляторных механизмов образования биопленки штаммами V. cholerae, а также сигналам внешней среды, являющимся триггером при ее формировании. в данном обзоре приведены ранее полученные сведения, а также новые данные о регуляторной сети V. cholerae, контролирующей процесс образования биопленки, включающей транскрипционные активаторы, репрессоры, альтернативные сигма-факторы, регуляторные РНК и ряд сигнальных молекул. отмечено также участие регуляторных механизмов при формировании биопленки в макроорганизме. представлены данные о сигналах внешней среды (наличие питательных веществ (углеводов), желчи, неорганических веществ, изменение осмолярности среды), стимулирующих/подавляющих ее формирование. учитывая решающую роль экзополисахарида в процессе образования зрелой биопленки, а также важную роль сигнальных молекул системы Quorum Sensing и 3'-5'-циклического дигуанилатмонофосфата в данном процессе, особое внимание уделено рассмотрению механизмов биосинтеза экзополисахарида и действию указанных сигнальных молекул.

Currently it is a common knowledge that the ability of cholera agent to form biofilm increases the survival rate and persistence both in external environment and macroorganism. V. cholerae cells in associated state are better protected from the effect of a range of factors, more effectively consume nutrient substances and exchange genetic information. The process of biofilm formation by cholera vibrio is investigated in sufficient detail. However, taking into consideration the significant role of this structure in the life cycle of V. cholerae, researchers obtain new data and clarify earlier gathered information on the molecular mechanisms that lie at the bottom of this process, using advanced analytical methods. Herewith, close attention is paid to studies of regulatory mechanisms of biofilm formation, as well as external environment signals that trigger it. This review presents previously obtained data and new information on V cholerae regulatory network, controlling the process of biofilm formation, including transcriptional activators, repressors, alternative sigma-factors, regulatory RNA, and a range of signal molecules. The role of regulatory mechanisms in biofilm formation inside a macroorganism is also considered in the paper. Given are the data on external environment signals (availability of nutrient substances (carbohydrates), bile, non-organic substances; change in osmolarity of the media), stimulating/suppressing its formation. Taking into account the critical role of exopolysaccharide in mature biofilm formation, as well as significant role of signal molecules of Quorum Sensing system and 3'-5'-cyclic diguanylate monophosphate in the process, a particular attention is drawn to mechanisms of exopolysaccharide biosynthesis and effect of the mentioned molecules.

Vibrio choleraeбиопленка3'-5'-циклический дигуанилатмонофосфатQuorum-Sensing

Vibrio choleraebiofilm3'-5'-cyclic diguanylate monophosphateQuorum-Sensing

References1

Lasa I. Towards the identification of the common features of bacterial biofilm development. Int. Microbiol. 2006; 9(1):21-8. PMID: 16636986.

Faruque S.M., Biswas K., Udden S.M., Ahmad Q.S., Sack D.A., Nair G.B., Mekalanos J.J. Transmissibility of cholera: in vivoformed biofilms and their relationship to infectivity and persistence in the environment. Proc. Natl. Acad. Sci. USA. 2006; 103(16):6350-5. DOI: 10.1073/pnas.0601277103.

Faruque S.M., Nair G.B. Vibrio cholerae: Genomics and molecular biology. Caister Academic Press, Norfolk, UK: Horizon Scientific Press; 2008. 218 p.

Alam A., Larocque R.C., Harris J.B., Vanderspurt C., Ryan E.T., Qadri F., Calderwood S.B. Hyperinfectivity of human-passaged Vibrio cholerae can be modeled by growth in the infant mouse. Infect. Immun. 2005; 73(10):6674-9. DOI: 10.1128/IAI.73.10.6674-6679.2005.

Augustin M., Ali-Vehmas T., Atroshi F. Assessment of enzymatic cleaning agents and disinfectants against bacterial biofilms. J. Pharm. Pharmaceut. Sci. 2004;.7(1):55-64.

Chavez-Dozal A., Gorman C., Erken M., Steinberg P.D., McDougald D., Nishiguchi M.K. Predation response of Vibriofischeri biofilms to bacterivorus protists. Appl. Environ. Microbiol. 2013; 79(2):553-8. DOI: 10.1128/AEM.027r0-12.

Watnick P. J. Kolter R. Steps in the development of a Vibrio cholerae El Tor biofilm. Mol. Microbiol. 1999; 34(3):586-95. PMID: 10564499. PMCID: PMC2860543.

Meibom K.L., Blokesch M., Dolganov N.A., Wu C.Y., Schoolnik G.K. Chitin induces natural competence in Vibrio cholerae. Science. 2005; 310(5755):1824-7. DOI: 10.1126/science.U20096.

Wong G.C. Three-dimensional architecture of Vibrio cholerae biofilms. Proc. Natl. Acad. Sci. USA. 2016; 113(14):3711-3. DOI: 10.1073/pnas.1603016113.

Yildiz F.H., Schoolnik G.K. Vibrio cholerae O1 El Tor: identification of a gene cluster required for the rugose colony type, exopolysaccharide production, chlorine resistance, and biofilm formation. Proc. Natl. Acad. Sci. USA. 1999; 96(7):4028-33. DOI: 10.1073/pnas.96.7.4028.

Kirn T. J., Jude B.A., Taylor R.K. A colonization factor links Vibrio cholerae environmental survival and human infection. Nature. 2005; 438(7069):863-6. DOI: 10.1038/nature04249.

Van Dellen K.L., Watnick P.I. The Vibrio cholerae biofilm: а target for novel therapies to prevent and treat cholera. Drug Discovery Today Dis. Mech. 2006; 3(2):261-6. DOI: 10.1016/j.ddmec.2006.06.013.

Hung D.T Shakhnovich E.A., Pierson E., Mekalanos J.J. Small-molecule inhibitor of Vibrio cholerae virulence and intestinal colonization. Science. 2005; 310(5748):670-4. DOI: 10.1126/science.1116739.

Craig S.A. Regulation of biofilm formation and outer membrane protein expression in Vibrio cholerae by iron [dissertation]. Austin: The University of Texas; 2008. (Cited 18 Jan 2019). Available from: https://repositories.lib.utexas.edu/handle/2152/17845.

Srivastava D., Hsieh M.L., Khataokar A., Neiditch M.B., Waters C.M. Cyclic di-GMP inhibits Vibrio cholerae motility by re-pressing induction of transcription and inducing extracellular poly-saccharide production. Mol. Microbiol. 2013; 90(6):1262-76. DOI: 10.1111/mmi.12432.

Beyhan S., Tischler A.D., Camilli A., Yildiz F.H. Transcriptome and phenotypic responses of Vibrio cholerae to increased cyclic di-GMP level. J. Bacteriol. 2006; 188(10):3600-13. DOI: 10.1128/JB.188.10.3600-3613.2006.

Jonson G., Lebens M., Holmgren J. Cloning and sequenc¬ing of Vibrio cholerae mannose-sensitive haemagglutinin pilin gene: localization of mshA within a cluster of type 4 pilin genes. Mol. Microbiol. 1994; 13(1):109-18. DOI: 10.1111/j.1365-2958.1994.tb00406.x.

Roelofs K.G., Jones C.J., Helman S.R., Shang X., Orr M.W., Goodson J.R., Galperin M.Y., Yildiz F.H., Lee V.T. Systematic identification of cyclic-di-GMP binding proteins in Vibrio cholerae reveals a novel class of cyclic-di-GMP-binding ATPases associated with Type II secretion systems. PLoSPathog. 2015; 11(10):e1005232. DOI: 10.1371/journal.ppat.1005232.

Fong J.C., Syed K.A., Klose K.E., Yildiz F.H. Role of Vibrio polysaccharide (vps) genes in VPS production, biofilm formation and Vibrio cholerae pathogenesis. Microbiology. 2010; 156(Pt 9):2757-69. DOI: 10.1099/mic.0.040196-0.

Yildiz F.H., Dolganov N.A., Schoolnik G.K. VpsR, a member of the response regulators of the two-component regulatory systems, is required for expression of vps biosynthesis genes and EPS(ETr)-associated phenotypes in Vibrio cholerae O1 El Tor. J. Bacteriol. 2001; 183(5):1716-26. DOI: 10.1128/JB.183.5.1716-1726.2001.

Yildiz F.H., Visick K.L. Vibrio biofilms: so much the same yet so different. Trends Microbiol. 2009; 17(3):109-18. DOI: 10.1016/j.tim.2008.12.004.

Fong J.C., Karplus K., Schoolnik G.K., Yildiz F.H. Identification and characterization of RbmA, a novel protein required for the development of rugose colony morphology and biofilm structure in Vibrio cholerae. J. Bacteriol. 2006; 188(3):1049-59. DOI: 10.1128/JB.188.3.1049-1059.2006.

Casper-Lindley C., Yildiz F.H. VpsT is a transcriptional regulator required for expression of vps biosynthesis genes and the development of rugose colonial morphology in Vibrio cholerae O1 El Tor. J. Bacteriol. 2004; 186(51:1574-8. DOI: 10.1128/JB.186.5.1574-1578.2004.

Conner J.G., Teschler J.K., Jones C.J., Yildiz F.H. Staying alive: Vibrio cholerae s cycle of environmental survival, transmission, and dissemination. Microbiol. Spectr. 2016; 4(2):593-633. DOI: 10.1128/microbiolspec.VMBF-00f5-2015.

Srivastava D., Harris R.C., Waters C.M. Integration of cyclic di-GMP and quorum sensing in the control of vpsT and aphA in Vibrio cholerae. J. Bacteriol. 2011; 193(22):6331-41. DOI: 10.1128/JB.05167-11.

Conner J.G., Zamorano-Sanchez D., Park J.H., Sondermann H., Yildiz F.H. The ins and outs of cyclic di-GMP signaling in Vibrio cholerae. Curr. Opin. Microbiol. 2017; 36:20-9. DOI: 10.1016/j.mib.2017.01.002.

Waters C.M., Bassler B.L. Quorum sensing: cell-to-cell communication in bacteria. Annu. Rev. Cell. Dev. Biol. 2005; 21:319¬46. DOI: 10.1146/annurev.cellbio.21.012704.131001

Federle M.J., Bassler B.L. Interspecies communication in bacteria. J. Clin. Invest. 2003; 112(9):1291-9. DOI: 10.1172/JCI20195.

Miller M.B., Skorupski K., Lenz D.H., Taylor R.K., Bassler B.L. Parallel quorum sensing systems converge to regulate virulence in Vibrio cholerae. Cell. 2002; 110(3):303-14 PMID: 12176318.

Higgins D.A., Pomianek M.E., Kraml C.M., Taylor R.K., Semmelhack M.F., Bassler B.L. The major Vibrio cholerae autoinducer and its role in virulence factor production. Nature. 2007; 450(71711:883-6. DOI: 10.1038/nature06284.

Jung S.A., Chapman C.A., Ng W.L. Quadruple quorum-sensing inputs control Vibrio cholerae virulence and maintain system robustness. PLoSPathog. 2015; 11(4):e1004837. DOI: 10.1371/journal.ppat.1004837.

Lenz D.H., Mok K.C., Lilley B.N., Kulkarni R.V, Wingreen N.S., Bassler B.L. The small RNA chaperone Hfq and multiple small RNAs control quorum sensing in Vibrio harveyi and Vibrio cholerae. Cell. 2004; 118(1):69-82. DOI: 10.1016/j.cell.2004.06.009.

32 Lenz D.H., Mok K.C., Lilley B.N., Kulkarni R.V, Wingreen N.S., Bassler B.L. The small RNA chaperone Hfq and multiple small RNAs control quorum sensing in Vibrio harveyi and Vibrio cholerae. Cell. 2004; 118(1):69-82. DOI: 10.1016/j.cell.2004.06.009.

Hammer B.K., Bassler B.L. Quorum sensing controls bio-film formation in Vibrio cholerae. Mol. Microbiol. 2003; 50(1):101-4. DOI: 10.1046/j.1365-2958.2003.03688.x.

Teschler J., Zamorano-Sanchez D., Utada A.S., Warner C.J.A., Wong G.C.L., Lenington R.G., Yildiz F.H. Living in the matrix: assembly and control of Vibrio cholerae biofilms. Nat. Rev. Microbiol. 2015; 13:255-68. DOI: 10.1038/nrmicro3433.

Colwell R.R., Spira W.M. The ecology of Vibrio cholerae. In: Barua D., Greenough W.B., editors. Cholera. Current Topics in Infectious Disease. Springer, Boston, MA; 1992. P. 107-27.

Zegans M.E., Becker H.I., Budzik J., O’Toole G. The role of bacterial biofilms in ocular infections. DNA Cell Biol. 2002; 21(5-6):415-20. DOI: 10.1089/10445490260099700.

Haugo A.J., Watnick P.I. Vibrio cholerae CytR is a repressor of biofilm development. Mol. Microbiol. 2002; 45(2):471-83. DOI: 10.1046/j.1365-2958.2002.03023.x.

Pruzzo C., Tarsi R., Lleo M.M., Signoretto C., Zampini M., Pane L., Colwell R.R., Canepari P. Persistence of adhesive properties in Vibrio cholerae after long-term exposure to sea water. Environ. Microbiol. 2003; 5(10):850-8. DOI: 10.1046/j.1462-2920.2003.00498.x.

Hung D.T., Zhu J., Sturtevant D., Mekalanos J.J. Bile acids stimulate biofilm formation in Vibrio cholerae. Mol. Microbiol. 2006; 59(1):193-201. DOI: 10.1111/j.1365-2958.2005.04846.x.

Bilecen K., Yildiz F.H. Identification of a calcium-controlled negative regulatory system affecting Vibrio cholerae biofilm formation. Environ. Microbiol. 2009; 11(8):2015-29. DOI: 10.1111/j.1462-2920.2009.01923.x.

Pratt J.T., McDonough E., Camilli A. PhoB regulates motility, biofilms, and cyclic di-GMP in Vibrio cholerae. J. Bacteriol. 2009; 191(211:6632-42. DOI: 10.1128/JB.00708-09.

Hall-Stoodley L., Stoodley P. Evolving concepts in biofilm infections. Cell Microbiol. 2009; 11(7):1034-43. DOI: 10.1111/j.1462-5822.2009.01323.x.

Shikuma N.J., Yildiz F.H. Identification and characterization of OscR, a transcriptional regulator involved in osmolarity adaptation in Vibrio cholerae. J. Bacteriol. 2009; 191(13):4082-96. DOI: 10.1128/JB.01540-08.

Landini P., Antoniani D., Burgess J.G., Nijland R. Molecular mechanisms of compounds affecting bacterial biofilm formation and dispersal. Appl. Microbiol. Biotechnol. 2010; 86(3):813-23. DOI: 10.1007/s00253-010-2468-8.

Houot L., Chang S., Pickering B.S., Absalon C., Watnick P.I. The phosphoenolpyruvate phosphotransferase system regulates Vibrio cholerae biofilm formation through multiple independent pathways. J. Bacteriol. 2010; 192(12):3055-67. DOI: 10.1128/JB.00213-10.

Kotrba P., Inui M., Yukawa H.J. Bacterial phosphotrans-ferase system (PTS) in carbohydrate uptake and control of carbon metabolism. J. Biosci. Bioeng. 2001; 92(6):502-17. DOI: 10.1016/S1389-1723(01)80308-X.

Ymele-Leki P., Houot L., Watnick P.I. Mannitol and the mannitol-specific enzyme IIB subunit activate Vibrio cholerae biofilm formation. Appl. Environ. Microbiol. 2013; 79(15):4675-83. DOI: 10.1128/AEM01184-13.

Begley M., Gahan C.G., Hill C. The interaction between bacteria andbile. FEMS Microbiol. Rev. 2005; 29(4):625-51. DOI: 10.1016/j.femsre.2004.09.003.

Koestler B.J., Waters C.M. Intestinal GPS: bile and bicarbonate control cyclic di-GMP to provide Vibrio cholerae spatial cues within the small intestine. Gut. Microbes. 2014; 5(6):775-80. DOI: 10.4161/19490976.2014.985989.

Koestler B.J., Waters C.M. Bile acids and bicarbonate inversely regulate intracellular cyclic di-GMP in Vibrio cholerae. Infect. Immun. 2014; 82(7):3002-14. DOI: 10.1128/IAI.01664-14.

Mueller R.S., Beyhan S., Saini S.G., Yildiz F.H., Bartlett D.H. Indole acts as an extracellular cue regulating gene expression in Vibrio cholerae. J. Bacteriol. 2009; 191(11):3504-16. DOI: 10.1128/JB.01240-08.

Correll D.L., Phosphorus: a rate limiting nutrient in surface waters. Poult. Sci. 1999; 78(5):674-82. DOI: 10.1093/ps/78.5.674.

Lery L.M., Goulart C.L., Figueiredo F.R., Verdoorn K.S., Einicker-Lamas M., Gomes F.M., Machado E.A., Bisch P.M., von Kruger W.M. A comparative proteomic analysis of Vibrio cholerae O1 wild-type cells versus a phoB mutant showed that the PhoB/ PhoR system is required for full growth and rpoS expression under inorganic phosphate abundance. JProteomics. 2013; 86:1-15. DOI: 10.1016/j.mrot.2013.04.038.

Shikuma N.J., Davis K.R., Fong J.N., Yildiz F.H. The transcriptional regulator, CosR, controls compatible solute biosynthesis and transport, motility and biofilm formation in Vibrio cholerae. Environ. Microbiol. 2013; 15(5):1387-99. DOI: 10.1111/j.1462-2920.2012.02805.x.

Mey A.R., Payne S.M. Haem utilization in Vibrio cholerae involves multiple TonB-dependent haem receptors. Mol. Microbiol. 2001; 42(3):835-49. DOI: 10.1046/j.1365-2958.2001.02683.x.

Yildiz F.H., Liu X.S., Heydorn A., Schoolnik G.K. Molecular analysis of rugosity in a Vibrio cholerae O1 El Tor phase variant. Mol. Microbiol. 2004; 53(2):497-515. DOI: 10.1111/j.1365-2958.2004.04154.x.

Lim B., Beyhan S., Meir J., Yildiz F.H. Cyclic-diGMP signal transduction systems in Vibrio cholerae: modulation of rugosity and biofilm formation. Mol. Microbiol. 2006; 60(2):331-48. DOI: 10.1111/j.1365-2958.2006.05106.x.

The authors declare that there are no conflicts of interest present.