Reciprocal c-di-GMP signaling: Incomplete flagellum biogenesis triggers c-di-GMP signaling pathways that promote biofilm formation


Autoři: Daniel C. Wu aff001;  David Zamorano-Sánchez aff001;  Fernando A. Pagliai aff001;  Jin Hwan Park aff001;  Kyle A. Floyd aff001;  Calvin K. Lee aff002;  Giordan Kitts aff001;  Christopher B. Rose aff001;  Eric M. Bilotta aff002;  Gerard C. L. Wong aff002;  Fitnat H. Yildiz aff001
Působiště autorů: Department of Microbiology and Environmental Toxicology, University of California, Santa Cruz, California, United States of America aff001;  Department of Bioengineering, University of California, Los Angeles, California, United States of America aff002;  Department of Chemistry and Biochemistry, University of California, Los Angeles, California, United States of America aff003;  California Nano Systems Institute, University of California, Los Angeles, California, United States of America aff004
Vyšlo v časopise: Reciprocal c-di-GMP signaling: Incomplete flagellum biogenesis triggers c-di-GMP signaling pathways that promote biofilm formation. PLoS Genet 16(3): e32767. doi:10.1371/journal.pgen.1008703
Kategorie: Research Article
doi: 10.1371/journal.pgen.1008703

Souhrn

The assembly status of the V. cholerae flagellum regulates biofilm formation, suggesting that the bacterium senses a lack of movement to commit to a sessile lifestyle. Motility and biofilm formation are inversely regulated by the second messenger molecule cyclic dimeric guanosine monophosphate (c-di-GMP). Therefore, we sought to define the flagellum-associated c-di-GMP-mediated signaling pathways that regulate the transition from a motile to a sessile state. Here we report that elimination of the flagellum, via loss of the FlaA flagellin, results in a flagellum-dependent biofilm regulatory (FDBR) response, which elevates cellular c-di-GMP levels, increases biofilm gene expression, and enhances biofilm formation. The strength of the FDBR response is linked with status of the flagellar stator: it can be reversed by deletion of the T ring component MotX, and reduced by mutations altering either the Na+ binding ability of the stator or the Na+ motive force. Absence of the stator also results in reduction of mannose-sensitive hemagglutinin (MSHA) pilus levels on the cell surface, suggesting interconnectivity of signal transduction pathways involved in biofilm formation. Strains lacking flagellar rotor components similarly launched an FDBR response, however this was independent of the status of assembly of the flagellar stator. We found that the FDBR response requires at least three specific diguanylate cyclases that contribute to increased c-di-GMP levels, and propose that activation of biofilm formation during this response relies on c-di-GMP-dependent activation of positive regulators of biofilm production. Together our results dissect how flagellum assembly activates c-di-GMP signaling circuits, and how V. cholerae utilizes these signals to transition from a motile to a sessile state.

Klíčová slova:

Bacterial biofilms – Biofilms – Flagella – Flagellar motility – Gene expression – Pathogen motility – Regulator genes – Vibrio cholerae


Zdroje

1. Flemming H-C, Wingender J, Szewzyk U, Steinberg P, Rice SA, Kjelleberg S. Biofilms: an emergent form of bacterial life. Nat Rev Microbiol [Internet]. 2016 Sep 11 [cited 2018 May 28]; 14(9):563–75. Available from: http://www.nature.com/articles/nrmicro.2016.94 doi: 10.1038/nrmicro.2016.94 27510863

2. Guttenplan SB, Kearns DB. Regulation of flagellar motility during biofilm formation. FEMS Microbiol Rev. 2013 Nov;37(6):849–71. doi: 10.1111/1574-6976.12018 23480406

3. Terashima H, Kawamoto A, Morimoto Y V., Imada K, Minamino T. Structural differences in the bacterial flagellar motor among bacterial species. Biophys Physicobiology [Internet]. 2017 [cited 2019 Jul 17]; 14(0):191–8. Available from: http://www.ncbi.nlm.nih.gov/pubmed/29362704

4. Chen S, Beeby M, Murphy GE, Leadbetter JR, Hendrixson DR, Briegel A, et al. Structural diversity of bacterial flagellar motors. EMBO J [Internet]. 2011 Jul 20 [cited 2019 Jul 17]; 30(14):2972–81. Available from: http://www.ncbi.nlm.nih.gov/pubmed/21673657 doi: 10.1038/emboj.2011.186 21673657

5. Minamino T, Imada K. The bacterial flagellar motor and its structural diversity. Trends Microbiol [Internet]. 2015 May [cited 2019 Jul 17]; 23(5):267–74. Available from: http://www.ncbi.nlm.nih.gov/pubmed/25613993 doi: 10.1016/j.tim.2014.12.011 25613993

6. Römling U, Galperin MY, Gomelsky M. Cyclic di-GMP: the first 25 years of a universal bacterial second messenger. Microbiol Mol Biol Rev. 2013 Mar;77(1):1–52. doi: 10.1128/MMBR.00043-12 23471616

7. Jenal U, Reinders A, Lori C. Cyclic di-GMP: second messenger extraordinaire. Nat Rev Microbiol [Internet]. 2017 Feb 6 [cited 2017 May 29]; 15(5):271–84. Available from: http://www.ncbi.nlm.nih.gov/pubmed/28163311 doi: 10.1038/nrmicro.2016.190 28163311

8. Simm R, Morr M, Kader A, Nimtz M, Römling U. GGDEF and EAL domains inversely regulate cyclic di-GMP levels and transition from sessility to motility. Mol Microbiol. 2004 Aug;53(4):1123–34. doi: 10.1111/j.1365-2958.2004.04206.x 15306016

9. Ryjenkov DA, Tarutina M, Moskvin O V, Gomelsky M. Cyclic diguanylate is a ubiquitous signaling molecule in bacteria: insights into biochemistry of the GGDEF protein domain. J Bacteriol. 2005 Mar;187(5):1792–8. doi: 10.1128/JB.187.5.1792-1798.2005 15716451

10. Tamayo R, Tischler AD, Camilli A. The EAL Domain Protein VieA Is a Cyclic Diguanylate Phosphodiesterase. J Biol Chem [Internet]. 2005 Sep 30 [cited 2019 Aug 14]; 280(39):33324–30. Available from: http://www.ncbi.nlm.nih.gov/pubmed/16081414 doi: 10.1074/jbc.M506500200 16081414

11. Chan C, Paul R, Samoray D, Amiot NC, Giese B, Jenal U, et al. Structural basis of activity and allosteric control of diguanylate cyclase. Proc Natl Acad Sci. 2004 Dec;101(49):17084–9. doi: 10.1073/pnas.0406134101 15569936

12. Paul K, Nieto V, Carlquist WC, Blair DF, Harshey RM. The c-di-GMP binding protein YcgR controls flagellar motor direction and speed to affect chemotaxis by a “backstop brake” mechanism. Mol Cell. 2010 Apr;38(1):128–39. doi: 10.1016/j.molcel.2010.03.001 20346719

13. Boehm A, Kaiser M, Li H, Spangler C, Kasper CA, Ackermann M, et al. Second Messenger-Mediated Adjustment of Bacterial Swimming Velocity. Cell. 2010;141(1):107–16. doi: 10.1016/j.cell.2010.01.018 20303158

14. Fang X, Gomelsky M. A post-translational, c-di-GMP-dependent mechanism regulating flagellar motility. Mol Microbiol [Internet]. 2010 Apr 23 [cited 2018 May 1]; 76(5):1295–305. Available from: http://www.ncbi.nlm.nih.gov/pubmed/20444091 doi: 10.1111/j.1365-2958.2010.07179.x 20444091

15. Baraquet C, Harwood CS. Cyclic diguanosine monophosphate represses bacterial flagella synthesis by interacting with the Walker A motif of the enhancer-binding protein FleQ. Proc Natl Acad Sci U S A [Internet]. 2013 Nov 12 [cited 2016 Sep 26]; 110(46):18478–83. Available from: http://www.ncbi.nlm.nih.gov/pubmed/24167275 doi: 10.1073/pnas.1318972110 24167275

16. Srivastava D, Hsieh M-L, Khataokar A, Neiditch MB, Waters CM. Cyclic di-GMP inhibits Vibrio cholerae motility by repressing induction of transcription and inducing extracellular polysaccharide production. Mol Microbiol [Internet]. 2013 Dec [cited 2016 Sep 25]; 90(6):1262–76. Available from: doi: 10.1111/mmi.12432 24134710

17. Orr MW, Lee VT. A PilZ domain protein for chemotaxis adds another layer to c-di-GMP-mediated regulation of flagellar motility. Sci Signal [Internet]. 2016 Oct 18 [cited 2019 Jul 17];9(450):fs16–fs16. Available from: http://www.ncbi.nlm.nih.gov/pubmed/27811181

18. Kojima S, Yamamoto K, Kawagishi I, Homma M. The polar flagellar motor of Vibrio cholerae is driven by an Na+ motive force. J Bacteriol [Internet]. 1999 Mar [cited 2019 Jul 17]; 181(6):1927–30. Available from: http://www.ncbi.nlm.nih.gov/pubmed/10074090 10074090

19. Echazarreta MA, Klose KE. Vibrio Flagellar Synthesis. Front Cell Infect Microbiol [Internet]. 2019 May 1 [cited 2019 Jul 17]; 9:131. Available from: http://www.ncbi.nlm.nih.gov/pubmed/31119103 doi: 10.3389/fcimb.2019.00131 31119103

20. Li N, Kojima S, Homma M. Sodium-driven motor of the polar flagellum in marine bacteria Vibrio. Genes to Cells [Internet]. 2011 Oct [cited 2019 May 27]; 16(10):985–99. Available from: http://www.ncbi.nlm.nih.gov/pubmed/21895888 doi: 10.1111/j.1365-2443.2011.01545.x 21895888

21. Zhu S, Nishikino T, Hu B, Kojima S, Homma M, Liu J. Molecular architecture of the sheathed polar flagellum in Vibrio alginolyticus. Proc Natl Acad Sci [Internet]. 2017 Oct 10 [cited 2019 May 22]; 114(41):10966–71. Available from: http://www.pnas.org/lookup/doi/10.1073/pnas.1712489114 28973904

22. Zhu S, Nishikino T, Takekawa N, Terashima H, Kojima S, Imada K, et al. In situ structure of the Vibrio polar flagellum reveals distinct outer membrane complex and its specific interaction with the stator. J Bacteriol. 2019 Nov 25;

23. Prouty MG, Correa NE, Klose KE. The novel sigma54- and sigma28-dependent flagellar gene transcription hierarchy of Vibrio cholerae. Mol Microbiol [Internet]. 2001 Mar [cited 2016 Sep 25]; 39(6):1595–609. Available from: http://www.ncbi.nlm.nih.gov/pubmed/11260476 doi: 10.1046/j.1365-2958.2001.02348.x 11260476

24. Syed KA, Beyhan S, Correa N, Queen J, Liu J, Peng F, et al. The Vibrio cholerae flagellar regulatory hierarchy controls expression of virulence factors. J Bacteriol [Internet]. 2009 Nov [cited 2016 Sep 25]; 191(21):6555–70. Available from: http://www.ncbi.nlm.nih.gov/pubmed/19717600 doi: 10.1128/JB.00949-09 19717600

25. Dong TG, Mekalanos JJ. Characterization of the RpoN regulon reveals differential regulation of T6SS and new flagellar operons in Vibrio cholerae O37 strain V52. Nucleic Acids Res [Internet]. 2012 Sep [cited 2016 Sep 25]; 40(16):7766–75. Available from: http://www.ncbi.nlm.nih.gov/pubmed/22723378 doi: 10.1093/nar/gks567 22723378

26. Conner JG, Zamorano-Sánchez D, Park JH, Sondermann H, Yildiz FH. The ins and outs of cyclic di-GMP signaling in Vibrio cholerae. Curr Opin Microbiol [Internet]. 2017 Apr [cited 2017 Sep 10]; 36:20–9. Available from: http://www.ncbi.nlm.nih.gov/pubmed/28171809 doi: 10.1016/j.mib.2017.01.002 28171809

27. Jones CJ, Utada A, Davis KR, Thongsomboon W, Zamorano Sanchez D, Banakar V, et al. C-di-GMP Regulates Motile to Sessile Transition by Modulating MshA Pili Biogenesis and Near-Surface Motility Behavior in Vibrio cholerae. PLoS Pathog. 2015;11(10):1–27.

28. Roelofs KG, Jones CJ, Helman SR, Shang X, Orr MW, Goodson JR, et al. 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. PLoS Pathog [Internet]. 2015 Oct [cited 2016 Sep 25]; 11(10):e1005232. Available from: http://www.ncbi.nlm.nih.gov/pubmed/26506097 doi: 10.1371/journal.ppat.1005232 26506097

29. Pratt JT, Tamayo R, Tischler AD, Camilli A. PilZ domain proteins bind cyclic diguanylate and regulate diverse processes in Vibrio cholerae. J Biol Chem. 2008;148(4):825–32.

30. Liu X, Beyhan S, Lim B, Linington RG, Yildiz FH. Identification and characterization of a phosphodiesterase that inversely regulates motility and biofilm formation in Vibrio cholerae. J Bacteriol [Internet]. 2010 Sep [cited 2016 Sep 25]; 192(18):4541–52. Available from: http://www.ncbi.nlm.nih.gov/pubmed/20622061 doi: 10.1128/JB.00209-10 20622061

31. Teschler JK, Zamorano-Sánchez D, Utada AS, Warner CJA, Wong GCL, Linington RG, et al. Living in the matrix: assembly and control of Vibrio cholerae biofilms. Nat Rev Microbiol [Internet]. 2015 May [cited 2016 Sep 26]; 13(5):255–68. Available from: http://www.ncbi.nlm.nih.gov/pubmed/25895940 doi: 10.1038/nrmicro3433 25895940

32. Berk V, Fong JCN, Dempsey GT, Develioglu ON, Zhuang X, Liphardt J, et al. Molecular Architecture and Assembly Principles of Vibrio cholerae Biofilms. Science (80-) [Internet]. 2012 Jul 13 [cited 2018 Mar 28]; 337(6091):236–9. Available from: http://www.ncbi.nlm.nih.gov/pubmed/22798614

33. Smith DR, Maestre-Reyna M, Lee G, Gerard H, Wang AH-J, Watnick PI. In situ proteolysis of the Vibrio cholerae matrix protein RbmA promotes biofilm recruitment. Proc Natl Acad Sci [Internet]. 2015 Aug 18 [cited 2019 Jul 18]; 112(33):10491–6. Available from: http://www.ncbi.nlm.nih.gov/pubmed/26240338 doi: 10.1073/pnas.1512424112 26240338

34. Fong JC, Rogers A, Michael AK, Parsley NC, Cornell W-C, Lin Y-C, et al. Structural dynamics of RbmA governs plasticity of Vibrio cholerae biofilms. Elife [Internet]. 2017 Aug 1 [cited 2019 Jul 18];6. Available from: http://www.ncbi.nlm.nih.gov/pubmed/28762945

35. Yildiz FH, Schoolnik GK. 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 U S A [Internet]. 1999 Mar 30 [cited 2017 Feb 10]; 96(7):4028–33. Available from: http://www.ncbi.nlm.nih.gov/pubmed/10097157 doi: 10.1073/pnas.96.7.4028 10097157

36. Fong JCN, Syed KA, Klose KE, Yildiz FH. Role of Vibrio polysaccharide (vps) genes in VPS production, biofilm formation and Vibrio cholerae pathogenesis. Microbiology [Internet]. 2010 Sep 1 [cited 2017 Feb 13]; 156(9):2757–69. Available from: http://www.ncbi.nlm.nih.gov/pubmed/20466768

37. Fong JCN, Karplus K, Schoolnik GK, Yildiz FH. 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 16428409

38. Fong JCN, Yildiz FH. The rbmBCDEF gene cluster modulates development of rugose colony morphology and biofilm formation in Vibrio cholerae. J Bacteriol. 2007 Mar;189(6):2319–30. doi: 10.1128/JB.01569-06 17220218

39. Yildiz FH, Dolganov NA, Schoolnik GK. 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 Mar;183(5):1716–26. doi: 10.1128/JB.183.5.1716-1726.2001 11160103

40. Casper-Lindley C, Yildiz FH. 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 [Internet]. 2004 Mar [cited 2016 Sep 26]; 186(5):1574–8. Available from: http://www.ncbi.nlm.nih.gov/pubmed/14973043 doi: 10.1128/JB.186.5.1574-1578.2004 14973043

41. Srivastava D, Harris RC, Waters CM. Integration of cyclic di-GMP and quorum sensing in the control of vpsT and aphA in Vibrio cholerae. J Bacteriol [Internet]. 2011 Nov [cited 2016 Sep 26]; 193(22):6331–41. Available from: http://www.ncbi.nlm.nih.gov/pubmed/21926235 doi: 10.1128/JB.05167-11 21926235

42. Krasteva P V, Fong JCN, Shikuma NJ, Beyhan S, Navarro MVAS, Yildiz FH, et al. Vibrio cholerae VpsT regulates matrix production and motility by directly sensing cyclic di-GMP. Science [Internet]. 2010 Feb 12 [cited 2016 Sep 25]; 327(5967):866–8. Available from: http://www.ncbi.nlm.nih.gov/pubmed/20150502 doi: 10.1126/science.1181185 20150502

43. Waters CM, Lu W, Rabinowitz JD, Bassler BL. Quorum sensing controls biofilm formation in Vibrio cholerae through modulation of cyclic di-GMP levels and repression of vpsT. J Bacteriol [Internet]. 2008 Apr [cited 2016 Sep 25]; 190(7):2527–36. Available from: http://www.ncbi.nlm.nih.gov/pubmed/18223081 doi: 10.1128/JB.01756-07 18223081

44. Yildiz FH, Liu XS, Heydorn A, Schoolnik GK. Molecular analysis of rugosity in a Vibrio cholerae O1 El Tor phase variant. Mol Microbiol. 2004 Jul;53(2):497–515. doi: 10.1111/j.1365-2958.2004.04154.x 15228530

45. Lim B, Beyhan S, Meir J, Yildiz FH. Cyclic-diGMP signal transduction systems in Vibrio cholerae: modulation of rugosity and biofilm formation. Mol Microbiol [Internet]. 2006 Apr [cited 2016 Sep 25]; 60(2):331–48. Available from: http://www.ncbi.nlm.nih.gov/pubmed/16573684 doi: 10.1111/j.1365-2958.2006.05106.x 16573684

46. Beyhan S, Bilecen K, Salama SR, Casper-Lindley C, Yildiz FH. Regulation of rugosity and biofilm formation in Vibrio cholerae: comparison of VpsT and VpsR regulons and epistasis analysis of vpsT, vpsR, and hapR. J Bacteriol. 2007 Jan;189(2):388–402. doi: 10.1128/JB.00981-06 17071756

47. Ayala JC, Wang H, Silva AJ, Benitez JA. Repression by H-NS of genes required for the biosynthesis of the Vibrio cholerae biofilm matrix is modulated by the second messenger cyclic diguanylic acid. Mol Microbiol [Internet]. 2015 Aug [cited 2016 Sep 25]; 97(4):630–45. Available from: http://www.ncbi.nlm.nih.gov/pubmed/25982817 doi: 10.1111/mmi.13058 25982817

48. Wang H, Ayala JC, Silva AJ, Benitez JA. The Histone-Like Nucleoid Structuring Protein (H-NS) Is a Repressor of Vibrio cholerae Exopolysaccharide Biosynthesis (vps) Genes. Appl Environ Microbiol [Internet]. 2012 Apr 1 [cited 2017 Feb 16]; 78(7):2482–8. Available from: http://www.ncbi.nlm.nih.gov/pubmed/22287003 doi: 10.1128/AEM.07629-11 22287003

49. Zamorano-Sánchez D, Fong JCN, Kilic S, Erill I, Yildiz FH. Identification and Characterization of VpsR and VpsT Binding Sites in Vibrio cholerae. O’Toole GA, editor. J Bacteriol [Internet]. 2015 Apr 1 [cited 2018 May 28]; 197(7):1221–35. Available from: http://jb.asm.org/lookup/doi/10.1128/JB.02439-14 25622616

50. Watnick PI, Lauriano CM, Klose KE, Croal L, Kolter R. The absence of a flagellum leads to altered colony morphology, biofilm development and virulence in Vibrio cholerae O139. Mol Microbiol [Internet]. 2001 Jan [cited 2016 Sep 25]; 39(2):223–35. Available from: http://www.ncbi.nlm.nih.gov/pubmed/11136445 doi: 10.1046/j.1365-2958.2001.02195.x 11136445

51. Lauriano CM, Ghosh C, Correa NE, Klose KE. The sodium-driven flagellar motor controls exopolysaccharide expression in Vibrio cholerae. J Bacteriol [Internet]. 2004 Aug [cited 2016 Sep 25]; 186(15):4864–74. Available from: http://www.ncbi.nlm.nih.gov/pubmed/15262923 doi: 10.1128/JB.186.15.4864-4874.2004 15262923

52. Tischler AD, Camilli A. Cyclic diguanylate (c-di-GMP) regulates Vibrio cholerae biofilm formation. Mol Microbiol [Internet]. 2004 Jun 28 [cited 2019 Jun 2]; 53(3):857–69. Available from: http://www.ncbi.nlm.nih.gov/pubmed/15255898 doi: 10.1111/j.1365-2958.2004.04155.x 15255898

53. Beyhan S, Tischler AD, Camilli A, Yildiz FH. Transcriptome and phenotypic responses of Vibrio cholerae to increased cyclic di-GMP level. J Bacteriol [Internet]. 2006 May [cited 2016 Sep 25]; 188(10):3600–13. Available from: http://www.ncbi.nlm.nih.gov/pubmed/16672614 doi: 10.1128/JB.188.10.3600-3613.2006 16672614

54. Beyhan S, Yildiz FH. Smooth to rugose phase variation in Vibrio cholerae can be mediated by a single nucleotide change that targets c-di-GMP signalling pathway. Mol Microbiol. 2007 Feb;63(4):995–1007. doi: 10.1111/j.1365-2958.2006.05568.x 17233827

55. Kawagishi I, Imagawa M, Imae Y, McCarter L, Homma M. The sodium-driven polar flagellar motor of marine Vibrio as the mechanosensor that regulates lateral flagellar expression. Mol Microbiol [Internet]. 1996 May [cited 2019 Jul 22]; 20(4):693–9. Available from: http://www.ncbi.nlm.nih.gov/pubmed/8793868 doi: 10.1111/j.1365-2958.1996.tb02509.x 8793868

56. Cairns LS, Marlow VL, Bissett E, Ostrowski A, Stanley-Wall NR. A mechanical signal transmitted by the flagellum controls signalling in Bacillus subtilis. Mol Microbiol [Internet]. 2013 Sep [cited 2019 Jul 22];90(1):n/a-n/a. Available from: http://www.ncbi.nlm.nih.gov/pubmed/23888912

57. Baker AE, O’Toole GA. Bacteria, Rev Your Engines: Stator Dynamics Regulate Flagellar Motility. Margolin W, editor. J Bacteriol. 2017 Jun;199(12).

58. Vorburger T, Stein A, Ziegler U, Kaim G, Steuber J. Functional role of a conserved aspartic acid residue in the motor of the Na+-driven flagellum from Vibrio cholerae. Biochim Biophys Acta—Bioenerg [Internet]. 2009 Oct [cited 2019 Jun 4]; 1787(10):1198–204. Available from: http://www.ncbi.nlm.nih.gov/pubmed/19501041

59. Vorburger T, Nedielkov R, Brosig A, Bok E, Schunke E, Steffen W, et al. Role of the Na + -translocating NADH:quinone oxidoreductase in voltage generation and Na + extrusion in Vibrio cholerae. Biochim Biophys Acta—Bioenerg [Internet]. 2016 Apr [cited 2019 Jan 21]; 1857(4):473–82. Available from: http://www.ncbi.nlm.nih.gov/pubmed/26721205

60. Fukuoka H, Wada T, Kojima S, Ishijima A, Homma M. Sodium-dependent dynamic assembly of membrane complexes in sodium-driven flagellar motors. Mol Microbiol [Internet]. 2009 Feb [cited 2019 Jul 24]; 71(4):825–35. Available from: doi: 10.1111/j.1365-2958.2008.06569.x 19183284

61. Van Dellen KL, Houot L, Watnick PI. Genetic analysis of Vibrio cholerae monolayer formation reveals a key role for DeltaPsi in the transition to permanent attachment. J Bacteriol [Internet]. 2008 Dec 15 [cited 2019 Jun 4]; 190(24):8185–96. Available from: http://jb.asm.org/cgi/doi/10.1128/JB.00948-08 18849423

62. Shikuma NJ, Fong JCN, Yildiz FH. Cellular levels and binding of c-di-GMP control subcellular localization and activity of the Vibrio cholerae transcriptional regulator VpsT. PLoS Pathog [Internet]. 2012 [cited 2016 Sep 25]; 8(5):e1002719. Available from: http://www.ncbi.nlm.nih.gov/pubmed/22654664 doi: 10.1371/journal.ppat.1002719 22654664

63. Yamaichi Y, Bruckner R, Ringgaard S, Möll A, Cameron DE, Briegel A, et al. A multidomain hub anchors the chromosome segregation and chemotactic machinery to the bacterial pole. Genes Dev [Internet]. 2012 Oct 15 [cited 2019 Aug 20]; 26(20):2348–60. Available from: http://genesdev.cshlp.org/cgi/doi/10.1101/gad.199869.112 23070816

64. Beyhan S, Odell LS, Yildiz FH. Identification and characterization of cyclic diguanylate signaling systems controlling rugosity in Vibrio cholerae. J Bacteriol [Internet]. 2008 Nov [cited 2016 Sep 25]; 190(22):7392–405. Available from: http://www.ncbi.nlm.nih.gov/pubmed/18790873 doi: 10.1128/JB.00564-08 18790873

65. Shikuma NJ, Fong JCN, Odell LS, Perchuk BS, Laub MT, Yildiz FH. Overexpression of VpsS, a hybrid sensor kinase, enhances biofilm formation in Vibrio cholerae. J Bacteriol [Internet]. 2009 Aug [cited 2016 Sep 26]; 191(16):5147–58. Available from: http://www.ncbi.nlm.nih.gov/pubmed/19525342 doi: 10.1128/JB.00401-09 19525342

66. Lenz DH, Mok KC, Lilley BN, Kulkarni R V, Wingreen NS, Bassler BL. The Small RNA Chaperone Hfq and Multiple Small RNAs Control Quorum Sensing in Vibrio harveyi and Vibrio cholerae. Cell [Internet]. 2004 Jul 9 [cited 2017 Mar 2]; 118(1):69–82. Available from: http://www.ncbi.nlm.nih.gov/pubmed/15242645 doi: 10.1016/j.cell.2004.06.009 15242645

67. Liu Z, Miyashiro T, Tsou A, Hsiao A, Goulian M, Zhu J. Mucosal penetration primes Vibrio cholerae for host colonization by repressing quorum sensing. Proc Natl Acad Sci [Internet]. 2008 Jul 15 [cited 2019 Jul 9]; 105(28):9769–74. Available from: http://www.ncbi.nlm.nih.gov/pubmed/18606988 http://www.pnas.org/lookup/doi/10.1073/pnas.1904577116 18606988

68. Hug I, Deshpande S, Sprecher KS, Pfohl T, Jenal U. Second messenger–mediated tactile response by a bacterial rotary motor. Science (80-). 2017 Oct;358(6362):531–4.

69. Baker AE, Webster SS, Diepold A, Kuchma SL, Bordeleau E, Armitage JP, et al. Flagellar stators stimulate c-di-GMP production by Pseudomonas aeruginosa. J Bacteriol [Internet]. 2019 Jan 14 [cited 2019 Aug 12]; Available from: http://www.ncbi.nlm.nih.gov/pubmed/30642992

70. Wang Y-C, Chin K-H, Tu Z-L, He J, Jones CJ, Sanchez DZ, et al. Nucleotide binding by the widespread high-affinity cyclic di-GMP receptor MshEN domain. Nat Commun [Internet]. 2016 Aug 31 [cited 2017 May 29]; 7:12481. Available from: http://www.ncbi.nlm.nih.gov/pubmed/27578558 doi: 10.1038/ncomms12481 27578558

71. Sangermani M, Hug I, Sauter N, Pfohl T, Jenal U. Tad pili play a dynamic role in Caulobacter crescentus surface colonization. MBio. 2019 May 1;10(3).

72. Tsou AM, Cai T, Liu Z, Zhu J, Kulkarni R V. Regulatory targets of quorum sensing in Vibrio cholerae: evidence for two distinct HapR-binding motifs. Nucleic Acids Res [Internet]. 2009 May [cited 2016 Oct 3]; 37(8):2747–56. Available from: http://www.ncbi.nlm.nih.gov/pubmed/19276207 doi: 10.1093/nar/gkp121 19276207

73. Ferreira JL, Gao FZ, Rossmann FM, Nans A, Brenzinger S, Hosseini R, et al. γ-proteobacteria eject their polar flagella under nutrient depletion, retaining flagellar motor relic structures. Kearns DB, editor. PLoS Biol [Internet]. 2019 Mar 19 [cited 2019 Jul 9]; 17(3):e3000165. Available from: http://dx.plos.org/10.1371/journal.pbio.3000165 30889173

74. Zamorano-Sánchez D, Xian W, Lee CK, Salinas M, Thongsomboon W, Cegelski L, et al. Functional Specialization in Vibrio cholerae Diguanylate Cyclases: Distinct Modes of Motility Suppression and c-di-GMP Production. Peter Greenberg E, editor. MBio [Internet]. 2019 Apr 23 [cited 2019 Jul 7]; 10(2). Available from: http://www.ncbi.nlm.nih.gov/pubmed/31015332

75. Zhou H, Zheng C, Su J, Chen B, Fu Y, Xie Y, et al. Characterization of a natural triple-tandem c-di-GMP riboswitch and application of the riboswitch-based dual-fluorescence reporter. Sci Rep [Internet]. 2016 Feb 19 [cited 2017 Feb 4]; 6:20871. Available from: http://www.nature.com/articles/srep20871 doi: 10.1038/srep20871 26892868

76. Heydorn A, Nielsen AT, Hentzer M, Sternberg C, Givskov M, Ersbøll BK, et al. Quantification of biofilm structures by the novel computer program COMSTAT. Microbiology [Internet]. 2000 Oct 1 [cited 2017 Jul 3]; 146 (Pt 1(10):2395–407. Available from: http://mic.microbiologyresearch.org/content/journal/micro/10.1099/00221287-146-10-2395

77. Vorregaard M, Lyngby K. Comstat2 -a modern 3D image analysis environment for biofilms. 2008 [cited 2017 Jul 3]; Available from: www.imm.dtu.dk

78. Lee CK, de Anda J, Baker AE, Bennett RR, Luo Y, Lee EY, et al. Multigenerational memory and adaptive adhesion in early bacterial biofilm communities. Proc Natl Acad Sci U S A [Internet]. 2018 Apr 24 [cited 2018 Jun 7]; 115(17):4471–6. Available from: http://www.pnas.org/lookup/doi/10.1073/pnas.1720071115 29559526

79. Gardel CL, Mekalanos JJ. Alterations in Vibrio cholerae motility phenotypes correlate with changes in virulence factor expression. Infect Immun. 1996 Jun;64(6):2246–55. 8675334

80. Meibom KL, Blokesch M, Dolganov NA, Wu CY, Schoolnik GK. Microbiology: Chitin induces natural competence in Vibrio cholerae. Science (80-). 2005 Dec 16;310(5755):1824–7.


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