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 Pathogens

Volumn 11, Issue 10, 2015, Pages

  Roelofs, Kevin G ^a   Jones, Christopher J ^b   Helman, Sarah R ^a   Shang, Xiaoran ^a   Orr, Mona W ^a   Goodson, Jonathan R ^a   Galperin, Michael Y ^c   Yildiz, Fitnat H ^b   Lee, Vincent T ^a  

^a University of Maryland   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c NATIONAL INSTITUTES OF HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATASE; ALANINE; ARGININE; CARBENICILLIN; GENTAMICIN; HEMAGGLUTININ; PHOSPHODIESTERASE; BIS(3',5')-CYCLIC DIGUANYLIC ACID; CYCLIC GMP; FIMBRIA PROTEIN; MANNOSE BINDING LECTIN; MSHA PROTEIN, VIBRIO CHOLERAE; TYPE II SECRETION SYSTEM;

ARTICLE; ATPASE ACTIVITY ASSAY; BACTERIUM PILUS; CONFOCAL LASER MICROSCOPY; CYCLIC DI GMP; ENZYME LINKED IMMUNOSORBENT ASSAY; NONHUMAN; OPEN READING FRAME; PHYLOGENETIC TREE; PROTEIN EXPRESSION; PROTEIN PURIFICATION; PSEUDOMONAS AERUGINOSA; SECOND MESSENGER; TYPE II SECRETION SYSTEM; VIBRIO CHOLERAE; ANALOGS AND DERIVATIVES; FIMBRIA; METABOLISM; PHYSIOLOGY;

ADENOSINE TRIPHOSPHATASES; CYCLIC GMP; FIMBRIAE PROTEINS; FIMBRIAE, BACTERIAL; MANNOSE-BINDING LECTIN; OPEN READING FRAMES; TYPE II SECRETION SYSTEMS; VIBRIO CHOLERAE;

EID: 84946016384     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1005232     Document Type: Article

References (114)

1. Ross P, Weinhouse H, Aloni Y, Michaeli D, Ohana P, Mayer R, et al. Regulation of cellulose synthesis in Acetobacter xylinum by cyclic diguanylic acid. Nature. 1987;325:279–81. 18990795
2. Ross P, Mayer R, Benziman M, Cellulose biosynthesis and function in bacteria. Microbiol Rev. 1991;55(1):35–58. 2030672
3. Paul R, Weiser S, Amiot NC, Chan C, Schirmer T, Giese B, et al. Cell cycle-dependent dynamic localization of a bacterial response regulator with a novel di-guanylate cyclase output domain. Genes Dev. 2004;18(6):715–27. 15075296
4. 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 U S A. 2004;101(49):17084–9. 15569936
5. Tal R, Wong HC, Calhoon R, Gelfand D, Fear AL, Volman G, et al. Three cdg operons control cellular turnover of cyclic di-GMP in Acetobacter xylinum: genetic organization and occurrence of conserved domains in isoenzymes. J Bacteriol. 1998;180(17):4416–25. 9721278
6. Barends TR, Hartmann E, Griese JJ, Beitlich T, Kirienko NV, Ryjenkov DA, et al. Structure and mechanism of a bacterial light-regulated cyclic nucleotide phosphodiesterase. Nature. 2009;459(7249):1015–8. doi: 10.1038/nature07966 19536266
7. Ryan RP, Fouhy Y, Lucey JF, Crossman LC, Spiro S, He YW, et al. Cell-cell signaling in Xanthomonas campestris involves an HD-GYP domain protein that functions in cyclic di-GMP turnover. Proc Natl Acad Sci U S A. 2006;103(17):6712–7. 16611728
8. Bellini D, Caly DL, McCarthy Y, Bumann M, An SQ, Dow JM, et al. Crystal structure of an HD-GYP domain cyclic-di-GMP phosphodiesterase reveals an enzyme with a novel trinuclear catalytic iron centre. Mol Microbiol. 2014;91(1):26–38. doi: 10.1111/mmi.12447 24176013
9. Ross P, Aloni Y, Weinhouse C, Michaeli D, Weinberger-Ohana P, Meyer R, et al. An unusual guanyl oligonucleotide regulates cellulose synthesis in Acetobacter xylinum. FEBS Lett. 1985;186(2):191–6. 19160595
10. Ross P, Aloni Y, Weinhouse H, Michaeli D, Weinberger-Ohana P, Mayer R, et al. Control of cellulose synthesis Acetobacter xylinum. A unique guanyl oligonucleotide is the immediate activator of the cellulose synthase. Carbohydrate Research. 1986;149(1):101–17.
11. Morgan JL, McNamara JT, Zimmer J, Mechanism of activation of bacterial cellulose synthase by cyclic di-GMP. Nat Struct Mol Biol. 2014;21(5):489–96. doi: 10.1038/nsmb.2803 24704788
12. Galperin MY, A census of membrane-bound and intracellular signal transduction proteins in bacteria: bacterial IQ, extroverts and introverts. BMC Microbiol. 2005;5:35. 15955239
13. Romling U, Galperin MY, Gomelsky M, Cyclic di-GMP: the first 25 years of a universal bacterial second messenger. Microbiol Mol Biol Rev. 2013;77(1):1–52. doi: 10.1128/MMBR.00043-12 23471616
14. Hengge R, Principles of c-di-GMP signalling in bacteria. Nat Rev Microbiol. 2009;7(4):263–73. doi: 10.1038/nrmicro2109 19287449
15. Schirmer T, Jenal U, Structural and mechanistic determinants of c-di-GMP signalling. Nat Rev Microbiol. 2009;7(10):724–35. doi: 10.1038/nrmicro2203 19756011
16. Amikam D, Galperin MY, PilZ domain is part of the bacterial c-di-GMP binding protein. Bioinformatics. 2006;22(1):3–6. 16249258
17. Merighi M, Lee VT, Hyodo M, Hayakawa Y, Lory S, The second messenger bis-(3'-5')-cyclic-GMP and its PilZ domain-containing receptor Alg44 are required for alginate biosynthesis in Pseudomonas aeruginosa. Mol Microbiol. 2007;65(4):876–95. 17645452
18. Pratt JT, Tamayo R, Tischler AD, Camilli A, PilZ domain proteins bind cyclic diguanylate and regulate diverse processes in Vibrio cholerae. J Biol Chem. 2007;282(17):12860–70. 17307739
19. Krasteva PV, Fong JC, Shikuma NJ, Beyhan S, Navarro MV, Yildiz FH, et al. Vibrio cholerae VpsT regulates matrix production and motility by directly sensing cyclic di-GMP. Science. 2010;327(5967):866–8. doi: 10.1126/science.1181185 20150502
20. 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. 2011;193(22):6331–41. doi: 10.1128/JB.05167-11 21926235
21. Srivastava D, Hsieh ML, 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. 2013;90(6):1262–76. doi: 10.1111/mmi.12432 24134710
22. Hickman JW, Harwood CS, Identification of FleQ from Pseudomonas aeruginosa as a c-di-GMP-responsive transcription factor. Mol Microbiol. 2008;69(2):376–89. doi: 10.1111/j.1365-2958.2008.06281.x 18485075
23. Leduc JL, Roberts GP, Cyclic di-GMP allosterically inhibits the CRP-like protein (Clp) of Xanthomonas axonopodis pv. citri. J Bacteriol. 2009;191(22):7121–2. doi: 10.1128/JB.00845-09 19633082
24. Tao F, He YW, Wu DH, Swarup S, Zhang LH, The cyclic nucleotide monophosphate domain of Xanthomonas campestris global regulator Clp defines a new class of cyclic di-GMP effectors. J Bacteriol. 2010;192(4):1020–9. doi: 10.1128/JB.01253-09 20008070
25. Tschowri N, Schumacher MA, Schlimpert S, Chinnam NB, Findlay KC, Brennan RG, et al. Tetrameric c-di-GMP mediates effective transcription factor dimerization to control Streptomyces development. Cell. 2014;158(5):1136–47. doi: 10.1016/j.cell.2014.07.022 25171413
26. Christen B, Christen M, Paul R, Schmid F, Folcher M, Jenoe P, et al. Allosteric control of cyclic di-GMP signaling. J Biol Chem. 2006;281(42):32015–24. 16923812
27. Galperin MY, Nikolskaya AN, Koonin EV, Novel domains of the prokaryotic two-component signal transduction systems. FEMS Microbiol Lett. 2001;203(1):11–21. 11557134
28. Newell PD, Monds RD, O'Toole GA, LapD is a bis-(3',5')-cyclic dimeric GMP-binding protein that regulates surface attachment by Pseudomonas fluorescens Pf0-1. Proc Natl Acad Sci U S A. 2009;106(9):3461–6. doi: 10.1073/pnas.0808933106 19218451
29. Navarro MV, De N, Bae N, Wang Q, Sondermann H, Structural analysis of the GGDEF-EAL domain-containing c-di-GMP receptor FimX. Structure. 2009;17(8):1104–16. doi: 10.1016/j.str.2009.06.010 19679088
30. Schmidt AJ, Ryjenkov DA, Gomelsky M, The ubiquitous protein domain EAL is a cyclic diguanylate-specific phosphodiesterase: enzymatically active and inactive EAL domains. J Bacteriol. 2005;187(14):4774–81. 15995192
31. Lee VT, Matewish JM, Kessler JL, Hyodo M, Hayakawa Y, Lory S, A cyclic-di-GMP receptor required for bacterial exopolysaccharide production. Mol Microbiol. 2007;65(6):1474–84. 17824927
32. Chin KH, Lee YC, Tu ZL, Chen CH, Tseng YH, Yang JM, et al. The cAMP receptor-like protein CLP is a novel c-di-GMP receptor linking cell-cell signaling to virulence gene expression in Xanthomonas campestris. J Mol Biol. 2010;396(3):646–62. doi: 10.1016/j.jmb.2009.11.076 20004667
33. Duvel J, Bertinetti D, Moller S, Schwede F, Morr M, Wissing J, et al. A chemical proteomics approach to identify c-di-GMP binding proteins in Pseudomonas aeruginosa. J Microbiol Methods. 2012;88(2):229–36. doi: 10.1016/j.mimet.2011.11.015 22178430
34. Nesper J, Reinders A, Glatter T, Schmidt A, Jenal U, A novel capture compound for the identification and analysis of cyclic di-GMP binding proteins. Journal of proteomics. 2012;75(15):4874–8. doi: 10.1016/j.jprot.2012.05.033 22652488
35. An SQ, Caly DL, McCarthy Y, Murdoch SL, Ward J, Febrer M, et al. Novel cyclic di-GMP effectors of the YajQ protein family control bacterial virulence. PLoS pathogens. 2014;10(10):e1004429. doi: 10.1371/journal.ppat.1004429 25329577
36. Corrigan RM, Campeotto I, Jeganathan T, Roelofs KG, Lee VT, Grundling A, Systematic identification of conserved bacterial c-di-AMP receptor proteins. Proc Natl Acad Sci U S A. 2013;110(22):9084–9. doi: 10.1073/pnas.1300595110 23671116
37. Huynh TN, Luo S, Pensinger D, Sauer JD, Tong L, Woodward JJ, An HD-domain phosphodiesterase mediates cooperative hydrolysis of c-di-AMP to affect bacterial growth and virulence. Proc Natl Acad Sci U S A. 2015;112(7):E747–56. doi: 10.1073/pnas.1416485112 25583510
38. Sureka K, Choi PH, Precit M, Delince M, Pensinger DA, Huynh TN, et al. The cyclic dinucleotide c-di-AMP is an allosteric regulator of metabolic enzyme function. Cell. 2014;158(6):1389–401. doi: 10.1016/j.cell.2014.07.046 25215494
39. Roelofs KG, Wang J, Sintim HO, Lee VT, Differential radial capillary action of ligand assay for high-throughput detection of protein-metabolite interactions. Proc Natl Acad Sci U S A. 2011;108(37):15528–33. doi: 10.1073/pnas.1018949108 21876132
40. Fang X, Ahmad I, Blanka A, Schottkowski M, Cimdins A, Galperin MY, et al. GIL, a new c-di-GMP-binding protein domain involved in regulation of cellulose synthesis in enterobacteria. Mol Microbiol. 2014;93(3):439–52. doi: 10.1111/mmi.12672 24942809
41. Rolfs A, Montor WR, Yoon SS, Hu Y, Bhullar B, Kelley F, et al. Production and sequence validation of a complete full length ORF collection for the pathogenic bacterium Vibrio cholerae. Proc Natl Acad Sci U S A. 2008;105(11):4364–9. doi: 10.1073/pnas.0712049105 18337508
42. Tischler AD, Camilli A, Cyclic diguanylate (c-di-GMP) regulates Vibrio cholerae biofilm formation. Mol Microbiol. 2004;53(3):857–69. 15255898
43. Tischler AD, Camilli A, Cyclic diguanylate regulates Vibrio cholerae virulence gene expression. Infect Immun. 2005;73(9):5873–82. 16113306
44. Koestler BJ, Waters CM, 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 24799624
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. 2006;60(2):331–48. 16573684
46. Schild S, Tamayo R, Nelson EJ, Qadri F, Calderwood SB, Camilli A, Genes induced late in infection increase fitness of Vibrio cholerae after release into the environment. Cell host & microbe. 2007;2(4):264–77. 18005744
47. Massie JP, Reynolds EL, Koestler BJ, Cong JP, Agostoni M, Waters CM, Quantification of high-specificity cyclic diguanylate signaling. Proc Natl Acad Sci U S A. 2012;109(31):12746–51. doi: 10.1073/pnas.1115663109 22802636
48. Finn RD, Bateman A, Clements J, Coggill P, Eberhardt RY, Eddy SR, et al. Pfam: the protein families database. Nucleic Acids Res. 2014;42(Database issue):D222–30. doi: 10.1093/nar/gkt1223 24288371
49. Hammer BK, Bassler BL, Distinct sensory pathways in Vibrio cholerae El Tor and classical biotypes modulate cyclic dimeric GMP levels to control biofilm formation. J Bacteriol. 2009;191(1):169–77. doi: 10.1128/JB.01307-08 18952786
50. Hartley JL, Temple GF, Brasch MA, DNA cloning using in vitro site-specific recombination. Genome Res. 2000;10(11):1788–95. 11076863
51. Benach J, Swaminathan SS, Tamayo R, Handelman SK, Folta-Stogniew E, Ramos JE, et al. The structural basis of cyclic diguanylate signal transduction by PilZ domains. Embo J. 2007;26(24):5153–66. 18034161
52. Kapust RB, Waugh DS, Escherichia coli maltose-binding protein is uncommonly effective at promoting the solubility of polypeptides to which it is fused. Protein Sci. 1999;8(8):1668–74. 10452611
53. Raran-Kurussi S, Waugh DS, The ability to enhance the solubility of its fusion partners is an intrinsic property of maltose-binding protein but their folding is either spontaneous or chaperone-mediated. PloS one. 2012;7(11):e49589. doi: 10.1371/journal.pone.0049589 23166722
54. Pugsley AP, The complete general secretory pathway in gram-negative bacteria. Microbiol Rev. 1993;57(1):50–108. 8096622
55. Peabody CR, Chung YJ, Yen MR, Vidal-Ingigliardi D, Pugsley AP, Saier MH, JrType II protein secretion and its relationship to bacterial type IV pili and archaeal flagella. Microbiology. 2003;149(Pt 11):3051–72. 14600218
56. Turner LR, Lara JC, Nunn DN, Lory S, Mutations in the consensus ATP-binding sites of XcpR and PilB eliminate extracellular protein secretion and pilus biogenesis in Pseudomonas aeruginosa. J Bacteriol. 1993;175(16):4962–9. 8102361
57. Turner LR, Olson JW, Lory S, The XcpR protein of Pseudomonas aeruginosa dimerizes via its N-terminus. Mol Microbiol. 1997;26(5):877–87. 9426126
58. Burrows LL, Pseudomonas aeruginosa twitching motility: type IV pili in action. Annu Rev Microbiol. 2012;66:493–520. doi: 10.1146/annurev-micro-092611-150055 22746331
59. Robien MA, Krumm BE, Sandkvist M, Hol WG, Crystal structure of the extracellular protein secretion NTPase EpsE of Vibrio cholerae. J Mol Biol. 2003;333(3):657–74. 14556751
60. Camberg JL, Sandkvist M, Molecular analysis of the Vibrio cholerae type II secretion ATPase EpsE. J Bacteriol. 2005;187(1):249–56. 15601709
61. Camberg JL, Johnson TL, Patrick M, Abendroth J, Hol WG, Sandkvist M, Synergistic stimulation of EpsE ATP hydrolysis by EpsL and acidic phospholipids. EMBO J. 2007;26(1):19–27. 17159897
62. Patrick M, Korotkov KV, Hol WG, Sandkvist M, Oligomerization of EpsE coordinates residues from multiple subunits to facilitate ATPase activity. J Biol Chem. 2011;286(12):10378–86. doi: 10.1074/jbc.M110.167031 21209100
63. Lu C, Turley S, Marionni ST, Park YJ, Lee KK, Patrick M, et al. Hexamers of the type II secretion ATPase GspE from Vibrio cholerae with increased ATPase activity. Structure. 2013;21(9):1707–17. doi: 10.1016/j.str.2013.06.027 23954505
64. Heidelberg JF, Eisen JA, Nelson WC, Clayton RA, Gwinn ML, Dodson RJ, et al. DNA sequence of both chromosomes of the cholera pathogen Vibrio cholerae. Nature. 2000;406(6795):477–83. 10952301
65. Giltner CL, Nguyen Y, Burrows LL, Type IV pilin proteins: versatile molecular modules. Microbiol Mol Biol Rev. 2012;76(4):740–72. doi: 10.1128/MMBR.00035-12 23204365
66. Stover CK, Pham XQ, Erwin AL, Mizoguchi SD, Warrener P, Hickey MJ, et al. Complete genome sequence of Pseudomonas aeruginosa PA01, an opportunistic pathogen. Nature. 2000;406(6799):959–64. 10984043
67. Lee DG, Urbach JM, Wu G, Liberati NT, Feinbaum RL, Miyata S, et al. Genomic analysis reveals that Pseudomonas aeruginosa virulence is combinatorial. Genome biology. 2006;7(10):R90. 17038190
68. Watnick PI, Kolter R, Steps in the development of a Vibrio cholerae El Tor biofilm. Mol Microbiol. 1999;34(3):586–95. 10564499
69. Utada AS, Bennett RR, Fong JC, Gibiansky ML, Yildiz FH, Golestanian R, et al. Vibrio cholerae use pili and flagella synergistically to effect motility switching and conditional surface attachment. Nature communications. 2014;5:4913. doi: 10.1038/ncomms5913 25234699
70. Campeotto I, Zhang Y, Mladenov MG, Freemont PS, Grundling A, Complex structure and biochemical characterization of the Staphylococcus aureus cyclic diadenylate monophosphate (c-di-AMP)-binding protein PstA, the founding member of a new signal transduction protein family. J Biol Chem. 2015;290(5):2888–901. doi: 10.1074/jbc.M114.621789 25505271
71. Muller M, Hopfner KP, Witte G, c-di-AMP recognition by Staphylococcus aureus PstA. FEBS Lett. 2015;589(1):45–51. doi: 10.1016/j.febslet.2014.11.022 25435171
72. Choi PH, Sureka K, Woodward JJ, Tong L, Molecular basis for the recognition of cyclic-di-AMP by PstA, a PII -like signal transduction protein. Microbiologyopen. 2015;4(3):361–74. doi: 10.1002/mbo3.243 25693966
73. Kim H, Youn SJ, Kim SO, Ko J, Lee JO, Choi BS, Structural Studies of Potassium Transport Protein KtrA Regulator of Conductance of K+ (RCK) C domain in Complex with Cyclic Diadenosine Monophosphate (c-di-AMP). J Biol Chem. 2015. 25957408
74. Moscoso JA, Schramke H, Zhang Y, Tosi T, Dehbi A, Jung K, et al. Binding of c-di-AMP to the Staphylococcus aureus sensor kinase KdpD occurs via the USP domain and down-regulates the expression of the Kdp potassium transporter. J Bacteriol. 2015. 26195599
75. Solano C, Garcia B, Latasa C, Toledo-Arana A, Zorraquino V, Valle J, et al. Genetic reductionist approach for dissecting individual roles of GGDEF proteins within the c-di-GMP signaling network in Salmonella. Proc Natl Acad Sci U S A. 2009;106(19):7997–8002. doi: 10.1073/pnas.0812573106 19416883
76. Gao X, Mukherjee S, Matthews PM, Hammad LA, Kearns DB, Dann CE, 3rdFunctional characterization of core components of the Bacillus subtilis cyclic-di-GMP signaling pathway. J Bacteriol. 2013;195(21):4782–92. doi: 10.1128/JB.00373-13 23893111
77. Abendroth J, Murphy P, Sandkvist M, Bagdasarian M, Hol WG, The X-ray structure of the type II secretion system complex formed by the N-terminal domain of EpsE and the cytoplasmic domain of EpsL of Vibrio cholerae. J Mol Biol. 2005;348(4):845–55. 15843017
78. Chen Y, Shiue SJ, Huang CW, Chang JL, Chien YL, Hu NT, et al. Structure and function of the XpsE N-terminal domain, an essential component of the Xanthomonas campestris type II secretion system. J Biol Chem. 2005;280(51):42356–63. 16162504
79. Marchler-Bauer A, Derbyshire MK, Gonzales NR, Lu S, Chitsaz F, Geer LY, et al. CDD: NCBI's conserved domain database. Nucleic Acids Res. 2015;43(Database issue):D222–6. doi: 10.1093/nar/gku1221 25414356
80. Chiavelli DA, Marsh JW, Taylor RK, The mannose-sensitive hemagglutinin of Vibrio cholerae promotes adherence to zooplankton. Appl Environ Microbiol. 2001;67(7):3220–5. 11425745
81. Zampini M, Canesi L, Betti M, Ciacci C, Tarsi R, Gallo G, et al. Role for mannose-sensitive hemagglutinin in promoting interactions between Vibrio cholerae El Tor and mussel hemolymph. Appl Environ Microbiol. 2003;69(9):5711–5. 12957968
82. Kamruzzaman M, Udden SM, Cameron DE, Calderwood SB, Nair GB, Mekalanos JJ, et al. Quorum-regulated biofilms enhance the development of conditionally viable, environmental Vibrio cholerae. Proc Natl Acad Sci U S A. 2010;107(4):1588–93. doi: 10.1073/pnas.0913404107 20080633
83. Watnick PI, Fullner KJ, Kolter R, A role for the mannose-sensitive hemagglutinin in biofilm formation by Vibrio cholerae El Tor. J Bacteriol. 1999;181(11):3606–9. 10348878
84. Zhu J, Mekalanos JJ, Quorum sensing-dependent biofilms enhance colonization in Vibrio cholerae. Dev Cell. 2003;5(4):647–56. 14536065
85. Hung DT, Zhu J, Sturtevant D, Mekalanos JJ, Bile acids stimulate biofilm formation in Vibrio cholerae. Mol Microbiol. 2006;59(1):193–201. 16359328
86. Tacket CO, Taylor RK, Losonsky G, Lim Y, Nataro JP, Kaper JB, et al. Investigation of the roles of toxin-coregulated pili and mannose-sensitive hemagglutinin pili in the pathogenesis of Vibrio cholerae O139 infection. Infect Immun. 1998;66(2):692–5. 9453628
87. Thelin KH, Taylor RK, Toxin-coregulated pilus, but not mannose-sensitive hemagglutinin, is required for colonization by Vibrio cholerae O1 El Tor biotype and O139 strains. Infect Immun. 1996;64(7):2853–6. 8698524
88. Hsiao A, Liu Z, Joelsson A, Zhu J, Vibrio cholerae virulence regulator-coordinated evasion of host immunity. Proc Natl Acad Sci U S A. 2006;103(39):14542–7. 16983078
89. Beyhan S, Odell LS, Yildiz FH, Identification and characterization of cyclic diguanylate signaling systems controlling rugosity in Vibrio cholerae. J Bacteriol. 2008;190(22):7392–405. doi: 10.1128/JB.00564-08 18790873
90. Kaufman MR, Seyer JM, Taylor RK, Processing of TCP pilin by TcpJ typifies a common step intrinsic to a newly recognized pathway of extracellular protein secretion by gram-negative bacteria. Genes Dev. 1991;5(10):1834–46. 1680773
91. Hsiao A, Toscano K, Zhu J, Post-transcriptional cross-talk between pro- and anti-colonization pili biosynthesis systems in Vibrio cholerae. Mol Microbiol. 2008;67(4):849–60. doi: 10.1111/j.1365-2958.2007.06091.x 18179420
92. Kazmierczak BI, Lebron MB, Murray TS, Analysis of FimX, a phosphodiesterase that governs twitching motility in Pseudomonas aeruginosa. Mol Microbiol. 2006;60(4):1026–43. 16677312
93. McCarthy Y, Ryan RP, O'Donovan K, He YQ, Jiang BL, Feng JX, et al. The role of PilZ domain proteins in the virulence of Xanthomonas campestris pv. campestris. Molecular plant pathology. 2008;9(6):819–24. doi: 10.1111/j.1364-3703.2008.00495.x 19019010
94. Guzzo CR, Salinas RK, Andrade MO, Farah CS, PILZ protein structure and interactions with PILB and the FIMX EAL domain: implications for control of type IV pilus biogenesis. J Mol Biol. 2009;393(4):848–66. doi: 10.1016/j.jmb.2009.07.065 19646999
95. Alm RA, Bodero AJ, Free PD, Mattick JS, Identification of a novel gene, pilZ, essential for type 4 fimbrial biogenesis in Pseudomonas aeruginosa. J Bacteriol. 1996;178(1):46–53. 8550441
96. Qi Y, Xu L, Dong X, Yau YH, Ho CL, Koh SL, et al. Functional divergence of FimX in PilZ binding and type IV pilus regulation. J Bacteriol. 2012;194(21):5922–31. doi: 10.1128/JB.00767-12 22942245
97. Chin KH, Kuo WT, Yu YJ, Liao YT, Yang MT, Chou SH, Structural polymorphism of c-di-GMP bound to an EAL domain and in complex with a type II PilZ-domain protein. Acta Crystallogr D Biol Crystallogr. 2012;68(Pt 10):1380–92. 22993092
98. Ryan RP, McCarthy Y, Kiely PA, O'Connor R, Farah CS, Armitage JP, et al. Dynamic complex formation between HD-GYP, GGDEF and PilZ domain proteins regulates motility in Xanthomonas campestris. Mol Microbiol. 2012;86(3):557–67. doi: 10.1111/mmi.12000 22924852
99. Baraquet C, Murakami K, Parsek MR, Harwood CS, The FleQ protein from Pseudomonas aeruginosa functions as both a repressor and an activator to control gene expression from the pel operon promoter in response to c-di-GMP. Nucleic Acids Res. 2012;40(15):7207–18. doi: 10.1093/nar/gks384 22581773
100. Beyhan S, Tischler AD, Camilli A, Yildiz FH, Transcriptome and phenotypic responses of Vibrio cholerae to increased cyclic di-GMP level. J Bacteriol. 2006;188(10):3600–13. 16672614
101. Andrews SC, Robinson AK, Rodriguez-Quinones F, Bacterial iron homeostasis. FEMS Microbiol Rev. 2003;27(2–3):215–37. 12829269
102. Chiang SM, Schellhorn HE, Regulators of oxidative stress response genes in Escherichia coli and their functional conservation in bacteria. Arch Biochem Biophys. 2012;525(2):161–9. doi: 10.1016/j.abb.2012.02.007 22381957
103. 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. 2004;186(5):1574–8. 14973043
104. Lu XH, An SQ, Tang DJ, McCarthy Y, Tang JL, Dow JM, et al. RsmA regulates biofilm formation in Xanthomonas campestris through a regulatory network involving cyclic di-GMP and the Clp transcription factor. PloS one. 2012;7(12):e52646. doi: 10.1371/journal.pone.0052646 23285129
105. Fazli M, McCarthy Y, Givskov M, Ryan RP, Tolker-Nielsen T, The exopolysaccharide gene cluster Bcam1330-Bcam1341 is involved in Burkholderia cenocepacia biofilm formation, and its expression is regulated by c-di-GMP and Bcam1349. Microbiologyopen. 2013;2(1):105–22. doi: 10.1002/mbo3.61 23281338
106. Sudarsan N, Lee ER, Weinberg Z, Moy RH, Kim JN, Link KH, et al. Riboswitches in eubacteria sense the second messenger cyclic di-GMP. Science. 2008;321(5887):411–3. doi: 10.1126/science.1159519 18635805
107. Lee ER, Baker JL, Weinberg Z, Sudarsan N, Breaker RR, An allosteric self-splicing ribozyme triggered by a bacterial second messenger. Science. 2010;329(5993):845–8. doi: 10.1126/science.1190713 20705859
108. Heydorn A, Nielsen AT, Hentzer M, Sternberg C, Givskov M, Ersboll BK, et al. Quantification of biofilm structures by the novel computer program COMSTAT. Microbiology. 2000;146 (Pt 10):2395–407. 11021916
109. Hunter JL, Severin GB, Koestler BJ, Waters CM, The Vibrio cholerae diguanylate cyclase VCA0965 has an AGDEF active site and synthesizes cyclic di-GMP. BMC Microbiol. 2014;14:22. doi: 10.1186/1471-2180-14-22 24490592
110. Tamayo R, Tischler AD, Camilli A, The EAL domain protein VieA is a cyclic diguanylate phosphodiesterase. J Biol Chem. 2005;280(39):33324–30. 16081414
111. Tamayo R, Schild S, Pratt JT, Camilli A, Role of cyclic Di-GMP during El Tor biotype Vibrio cholerae infection: characterization of the in vivo-induced cyclic Di-GMP phosphodiesterase CdpA. Infect Immun. 2008;76(4):1617–27. doi: 10.1128/IAI.01337-07 18227161
112. 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. 2010;192(18):4541–52. doi: 10.1128/JB.00209-10 20622061
113. 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. 2008;190(7):2527–36. doi: 10.1128/JB.01756-07 18223081
114. Pratt JT, McDonough E, Camilli A, PhoB regulates motility, biofilms, and cyclic di-GMP in Vibrio cholerae. J Bacteriol. 2009;191(21):6632–42. doi: 10.1128/JB.00708-09 19734314