Second messenger regulation of biofilm formation: Breakthroughs in understanding c-di-GMP effector systems

Annual Review of Cell and Developmental Biology

Volumn 28, Issue , 2012, Pages 439-462

  Boyd, Chelsea D ^a   O'Toole, George A ^a  

^a DARTMOUTH MEDICAL SCHOOL   (United States)

Author keywords

adhesion; diguanylate cyclase; exopolysaccharide; motility; phosphodiesterase

Indexed keywords

BIS(3' 5')CYCLIC DIMERIC GUANOSINE MONOPHOSPHATE; DIMER; GUANOSINE PHOSPHATE; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL CELL; BIODIVERSITY; BIOFILM; CELL ADHESION; CELL MOTILITY; CELL STRUCTURE; CELL SURFACE; CHEMICAL STRUCTURE; DIMERIZATION; ESCHERICHIA COLI; EXTRACELLULAR MATRIX; GENE EXPRESSION REGULATION; GENE MUTATION; INTRACELLULAR SIGNALING; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DEGRADATION; PROTEIN LOCALIZATION; PROTEIN SYNTHESIS; SECOND MESSENGER; SIGNAL TRANSDUCTION; TRANSCRIPTION REGULATION; VIRULENCE;

BIOFILMS; ESCHERICHIA COLI; FLAGELLA; GENE EXPRESSION REGULATION, BACTERIAL; GUANOSINE MONOPHOSPHATE; SECOND MESSENGER SYSTEMS; VIBRIO CHOLERAE;

BACTERIA (MICROORGANISMS);

EID: 84870208079     PISSN: 10810706     EISSN: 15308995     Source Type: Book Series    
DOI: 10.1146/annurev-cellbio-101011-155705     Document Type: Article

References (116)

1. Abel S, Chien P,Wassmann P, Schirmer T, Kaever V, et al. 2011. Regulatory cohesion of cell cycle and cell differentiation through interlinked phosphorylation and second messenger networks. Mol. Cell 43:550-60
2. Ahmad I, Lamprokostopoulou A, Le Guyon S, Streck E, Barthel M, et al. 2011. Complex c-di-GMP signaling networks mediate transition between virulence properties and biofilm formation in Salmonella enterica serovar Typhimurium. PLoS ONE 6:e28351
3. Amikam D, Galperin MY. 2006. PilZ domain is part of the bacterial c-di-GMP binding protein. Bioinformatics 22:3-6
4. Andrade MO, Alegria MC, Guzzo CR, Docena C, Rosa MC, et al. 2006. The HD-GYP domain of RpfG mediates a direct linkage between the Rpf quorum-sensing pathway and a subset of diguanylate cyclase proteins in the phytopathogen Xanthomonas axonopodis pv citri. Mol. Microbiol. 62:537-51
5. Barends TR, Hartmann E, Griese JJ, Beitlich T, Kirienko NV, et al. 2009. Structure and mechanism of a bacterial light-regulated cyclic nucleotide phosphodiesterase. Nature 459:1015-18
6. Benach J, Swaminathan SS, Tamayo R, Handelman SK, Folta-Stogniew E, et al. 2007. The structural basis of cyclic diguanylate signal transduction by PilZ domains. EMBO J. 26:5153-66
7. Bertin P, Terao E, Lee EH, Lejeune P, Colson C, et al. 1994. The H-NS protein is involved in the biogenesis of flagella in Escherichia coli. J. Bacteriol. 176:5537-40
8. Beyhan S, Bilecen K, Salama SR, Casper-Lindley C, Yildiz FH. 2007. 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. 189:388-402
9. Beyhan S, OdellLS, Yildiz FH. 2008. Identification and characterization of cyclic diguanylate signaling systems controlling rugosity in Vibrio cholerae. J. Bacteriol. 190:7392-405
10. Beyhan S, Tischler AD, Camilli A, Yildiz FH. 2006. Transcriptome and phenotypic responses of Vibrio cholerae to increased cyclic di-GMP level. J. Bacteriol. 188:3600-13
11. Beyhan S, Yildiz FH. 2007. 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. 63:995-1007
12. Bobrov AG, KirillinaO, Forman S,Mack D, Perry RD. 2008. Insights into Yersinia pestis biofilm development: topology and co-interaction ofHms inner membrane proteins involved in exopolysaccharide production. Environ. Microbiol. 10:1419-32
13. Boehm A, Kaiser M, Li H, Spangler C, Kasper CA, et al. 2010. Second messenger-mediated adjustment of bacterial swimming velocity. Cell 141:107-16
14. Boles BR, McCarter LL. 2002. Vibrio parahaemolyticus scrABC, a novel operon affecting swarming and capsular polysaccharide regulation. J. Bacteriol. 184:5946-54
15. Brown PN, Terrazas M, Paul K, Blair DF. 2007. Mutational analysis of the flagellar protein FliG: sites of interaction with FliM and implications for organization of the switch complex. J. Bacteriol. 189:305-12
16. Casper-Lindley C, Yildiz FH. 2004. 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. 186:1574-8
17. ChangAL, Tuckerman JR, GonzalezG,Mayer R, WeinhouseH, et al. 2001. Phosphodiesterase A1, a regulator of cellulose synthesis in Acetobacter xylinum, is a heme-based sensor. Biochemistry 40:3420-26
18. Chin KH, Lee YC, Tu ZL, Chen CH, Tseng YH, et al. 2010. 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. 396:646-62
19. Christen B, Christen M, Paul R, Schmid F, Folcher M, et al. 2006. Allosteric control of cyclic di-GMP signaling. J. Biol. Chem. 281:32015-24
20. Christen M, Christen B, Allan MG, Folcher M, Jeno P, et al. 2007. DgrA is a member of a new family of cyclic diguanosine monophosphate receptors and controls flagellar motor function in Caulobacter crescentus. Proc. Natl. Acad. Sci. USA 104:4112-17
21. Christen M, Christen B, Folcher M, Schauerte A, Jenal U. 2005. Identification and characterization of a cyclic di-GMP-specific phosphodiesterase and its allosteric control by GTP. J. Biol. Chem. 280:30829-37
22. Christen M, Kulasekara HD, Christen B, Kulasekara BR, Hoffman LR, Miller SI. 2010. Asymmetrical distribution of the second messenger c-di-GMP upon bacterial cell division. Science 328:1295-97
23. Costerton JW, Lewandowski Z,Caldwell DE,KorberDR, Lappin-ScottHM. 1995. Microbial biofilms. Annu. Rev. Microbiol. 49:711-45
24. Davey ME, O'Toole GA. 2000. Microbial biofilms: from ecology to molecular genetics. Microbiol. Mol. Biol. Rev. 64:847-67
25. Deflaun MF,Tanzer AS, McAteer AL,Marshall B, Levy SB. 1990. Development of an adhesion assay and characterization of an adhesion-deficient mutant of Pseudomonas fluorescens. Appl. Environ.Microbiol. 56:112-19
26. Donato GM, Kawula TH. 1998. Enhanced binding of altered H-NS protein to flagellar rotor protein FliG causes increased flagellar rotational speed and hypermotility in Escherichia coli. J. Biol. Chem. 273:24030-36
27. Duerig A, Abel S, Folcher M, NicollierM, Schwede T, et al. 2009. Second messenger-mediated spatiotemporal control of protein degradation regulates bacterial cell cycle progression. Genes Dev. 23:93-104
28. Fang X, Gomelsky M. 2010. A post-translational, c-di-GMP-dependent mechanism regulating flagellar motility. Mol. Microbiol. 76:1295-305
29. Fazli M, O'Connell A, NilssonM,Niehaus K,DowJM, et al. 2011. TheCRP/FNR family protein Bcam1349 is a c-di-GMP effector that regulates biofilm formation in the respiratory pathogen Burkholderia cenocepacia. Mol. Microbiol. 82:327-41
30. Ferreira RB, Antunes LC, Greenberg EP, McCarter LL. 2008. Vibrio parahaemolyticus ScrC modulates cyclic dimeric GMP regulation of gene expression relevant to growth on surfaces. J. Bacteriol. 190:851-60
31. Ferreira RBR, Chodur DM, Antunes LCM, Trimble MJ, McCarter LL. 2011. Output targets and transcriptional regulation by a cyclic dimeric GMP-responisve circuit in Vibrio parahaemolyticus Scr network. J. Bacteriol. 194:914-24
32. Freedman JC, Rogers EA, Kostick JL, Zhang H, Iyer R, et al. 2010. Identification and molecular characterization of a cyclic-di-GMP effector protein, PlzA (BB0733): additional evidence for the existence of a functional cyclic-di-GMP regulatory network in the Lyme disease spirochete, Borrelia burgdorferi. FEMS Immunol. Med. Microbiol. 58:285-94
33. Galperin MY, Nikolskaya AN, Koonin EV. 2001. Novel domains of the prokaryotic two-component signal transduction systems. FEMS Microbiol. Lett. 203:11-21
34. Genevaux P, Muller S, Bauda P. 1996. A rapid screening procedure to identify mini-Tn10 insertion mutants of Escherichia coli K-12 with altered adhesion properties. FEMS Microbiol. Lett. 142:27-30
35. Girgis HS, Liu Y, RyuWS, Tavazoie S. 2007. A comprehensive genetic characterization of bacterial motility. PLoS Genet. 3:1644-60
36. Guzzo CR, Salinas RK, Andrade MO, Farah CS. 2009. PILZ protein structure and interactions with PILB and the FIMX EAL domain: implications for control of type IV pilus biogenesis. J. Mol. Biol. 393:848-66
37. Habazettl J, Allan MG, Jenal U, Grzesiek S. 2011. Solution structure of the PilZ domain protein PA4608 complex with cyclic di-GMP identifies charge clustering as molecular readout. J. Biol. Chem. 286:14304-14
38. Hengge R. 2009. Principles of c-di-GMP signalling in bacteria. Nat. Rev. Microbiol. 7:263-73
39. Hickman JW, Harwood CS. 2008. Identification of FleQ from Pseudomonas aeruginosa as a c-di-GMPresponsive transcription factor. Mol. Microbiol. 69:376-89
40. Hickman JW,Tifrea DF,Harwood CS. 2005.Achemosensory system that regulates biofilm formation through modulation of cyclic diguanylate levels. Proc. Natl. Acad. Sci. USA 102:14422-27
41. Hinsa SM, Espinosa-Urgel M, Ramos JL, O'Toole GA. 2003. Transition from reversible to irreversible attachment during biofilm formation by Pseudomonas fluorescens WCS365 requires an ABC transporter and a large secreted protein. Mol. Microbiol. 49:905-18
42. Hinsa SM, O'Toole GA. 2006. Biofilm formation by Pseudomonas fluorescens WCS365: a role for LapD. Microbiology 152:1375-83
43. Hogan D, Kolter R. 2002. Why are bacteria refractory to antimicrobials? Curr. Opin. Microbiol. 5:472-77
44. Huang B,Whitchurch CB, Mattick JS. 2003. FimX, a multidomain protein connecting environmental signals to twitching motility in Pseudomonas aeruginosa. J. Bacteriol. 185:7068-76
45. Jackson DW, Simecka JW, Romeo T. 2002a. Catabolite repression of Escherichia coli biofilm formation. J. Bacteriol. 184:3406-10
46. JacksonDW, Suzuki K, Oakford L, Simecka JW,HartME, Romeo T. 2002b. Biofilm formation and dispersal under the influence of the global regulator CsrA of Escherichia coli. J. Bacteriol. 184:290-301
47. KaderA, SimmR,Gerstel U, Morr M, RomlingU. 2006. Hierarchical involvement of variousGGDEFdomain proteins in rdar morphotype development of Salmonella enterica serovar Typhimurium. Mol. Microbiol. 60:602-16
48. Kazmierczak BI, LebronMB, MurrayTS. 2006. Analysis of FimX, a phosphodiesterase that governs twitching motility in Pseudomonas aeruginosa. Mol. Microbiol. 60:1026-43
49. Ko J, Ryu KS, Kim H, Shin JS, Lee JO, et al. 2010. Structure of PP4397 reveals the molecular basis for different c-di-GMP binding modes by PilZ domain proteins. J. Mol. Biol. 398:97-110
50. Ko M, Park C. 2000. Two novel flagellar components and H-NS are involved in the motor function of Escherichia coli. J. Mol. Biol. 303:371-82
51. Krasteva PV, Fong JC, Shikuma NJ, Beyhan S,Navarro MV, et al. 2010. Vibrio cholerae VpsT regulates matrix production and motility by directly sensing cyclic di-GMP. Science 327:866-68
52. Kulshina N, Baird NJ, Ferre-D'Amare AR. 2009. Recognition of the bacterial second messenger cyclic diguanylate by its cognate riboswitch. Nat. Struct. Mol. Biol. 16:1212-17
53. Leduc JL, RobertsGP. 2009. Cyclic di-GMP allosterically inhibits the CRP-like protein (Clp) of Xanthomonas axonopodis pv. citri. J. Bacteriol. 191:7121-22
54. Lee ER, Baker JL, Weinberg Z, Sudarsan N, Breaker RR. 2010. An allosteric self-splicing ribozyme triggered by a bacterial second messenger. Science 329:845-48
55. Lee VT, Matewish JM, Kessler JL,Hyodo M, Hayakawa Y, Lory S. 2007. A cyclic-di-GMP receptor required for bacterial exopolysaccharide production. Mol. Microbiol. 65:1474-84
56. Lim B, Beyhan S, Meir J, Yildiz FH. 2006. Cyclic-diGMP signal transduction systems in Vibrio cholerae: modulation of rugosity and biofilm formation. Mol. Microbiol. 60:331-48
57. Lloyd SA, Blair DF. 1997. Charged residues of the rotor protein FliG essential for torque generation in the flagellar motor of Escherichia coli. J. Mol. Biol. 266:733-44
58. Lugtenberg BJ, Kravchenko LV, Simons M. 1999. Tomato seed and root exudate sugars: composition, utilization by Pseudomonas biocontrol strains and role in rhizosphere colonization. Environ. Microbiol. 1:439-46
59. Merighi M, Lee VT, Hyodo M, Hayakawa Y, Lory S. 2007. 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. 65:876-95
60. Merritt JH, Ha DG, Cowles KN, LuW, Morales DK, et al. 2010. Specific control of Pseudomonas aeruginosa surface-associated behaviors by two c-di-GMP diguanylate cyclases. mBio 1:e00183-10
61. Monds RD, Newell PD,Gross RH, O'Toole GA. 2007. Phosphate- dependentmodulation of c-di-GMP levels regulates Pseudomonas fluorescens Pf0-1 biofilm formation by controlling secretion of the adhesin LapA. Mol. Microbiol. 63:656-79
62. Navarro MV,DeN, Bae N, Wang Q, Sondermann H. 2009. Structural analysis of the GGDEF-EAL domaincontaining c-di-GMP receptor FimX. Structure 17:1104-16
63. Navarro MV, Newell PD, Krasteva PV, Chatterjee D, Madden DR, et al. 2011. Structural basis for c-di-GMP-mediated inside-out signaling controlling periplasmic proteolysis. PLoS Biol. 9:e1000588
64. Newell PD,BoydCD, Sondermann H, O'Toole GA. 2011a.Ac-di-GMP effector system controls cell adhesion by inside-out signaling and surface protein cleavage. PLoS Biol. 9:e1000587
65. Newell PD, Monds RD, O'Toole GA. 2009. LapD is a bis-(3-,5-)-cyclic dimeric GMP-binding protein that regulates surface attachment by Pseudomonas fluorescens Pf0-1. Proc. Natl. Acad. Sci. USA 106:3461-66
66. Newell PD, Yoshioka S, Hvorecny KL, Monds RD, O'Toole GA. 2011b. Systematic analysis of diguanylate cyclases that promote biofilm formation by Pseudomonas fluorescens Pf0-1. J. Bacteriol. 193:4685-98
67. Oglesby LL, Jain S, Ohman DE. 2008. Membrane topology and roles of Pseudomonas aeruginosa Alg8 and Alg44 in alginate polymerization. Microbiology 154:1605-15
68. O'Toole GA, Gibbs KA, Hager PW, Phibbs PV Jr, Kolter R. 2000. The global carbon metabolism regulator Crc is a component of a signal transduction pathway required for biofilm development by Pseudomonas aeruginosa. J. Bacteriol. 182:425-31
69. O'Toole GA, Kolter R. 1998a. Flagellar and twitching motility are necessary for Pseudomonas aeruginosa biofilm development. Mol. Microbiol. 30:295-304
70. O'Toole GA, Kolter R. 1998b. Initiation of biofilm formation in Pseudomonas fluorescens WCS365 proceeds via multiple, convergent signalling pathways: a genetic analysis. Mol. Microbiol. 28:449-61
71. Paul K, Nieto V, Carlquist WC, Blair DF,Harshey RM. 2010. The c-di-GMP binding protein YcgR controls flagellar motor direction and speed to affect chemotaxis by a backstop brake mechanism. Mol. Cell 38:128-39
72. Paul R, Abel S, Wassmann P, Beck A, Heerklotz H, Jenal U. 2007. Activation of the diguanylate cyclase PleD by phosphorylation-mediated dimerization. J. Biol. Chem. 282:29170-77
73. Paul R, Weiser S, Amiot NC, Chan C, Schirmer T, et al. 2004. Cell cycle-dependent dynamic localization of a bacterial response regulator with a novel di-guanylate cyclase output domain. Genes Dev. 18:715-27
74. Pitzer JE, Sultan SZ, Hayakawa Y, Hobbs G, MillerMR, MotalebMA. 2011. Analysis of the Borrelia burgdorferi cyclic-di-GMP-binding protein PlzA reveals a role in motility and virulence. Infect. Immun. 79:1815-25
75. 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
76. Pratt JT, Tamayo R, Tischler AD, Camilli A. 2007. PilZ domain proteins bind cyclic diguanylate and regulate diverse processes in Vibrio cholerae. J. Biol. Chem. 282:12860-70
77. Pratt LA, Kolter R. 1998. Genetic analysis of Escherichia coli biofilm formation: roles of flagella, motility, chemotaxis and type I pili. Mol. Microbiol. 30:285-93
78. Prigent-Combaret C, Brombacher E, Vidal O, Ambert A, Lejeune P, et al. 2001. Complex regulatory network controls initial adhesion and biofilm formation in Escherichia coli via regulation of the csgD gene. J. Bacteriol. 183:7213-23
79. Prigent-Combaret C, Vidal O, Dorel C, Lejeune P. 1999. Abiotic surface sensing and biofilm-dependent regulation of gene expression in Escherichia coli. J. Bacteriol. 181:5993-6002
80. Qi Y, Chuah ML, Dong X, Xie K, Luo Z, et al. 2011. Binding of cyclic diguanylate in the non-catalytic EAL domain of FimX induces a long-range conformational change. J. Biol. Chem. 286:2910-17
81. Qi Y, Rao F, Luo Z, Liang ZX. 2009. A flavin cofactor-binding PAS domain regulates c-di-GMP synthesis in AxDGC2 from Acetobacter xylinum. Biochemistry 48:10275-85
82. Rao F, Pasunooti S,Ng Y, ZhuoW, Lim L, et al. 2009. Enzymatic synthesis of c-di-GMP using a thermophilic diguanylate cyclase. Anal. Biochem. 389:138-42
83. RomlingU,GomelskyM,Galperin MY. 2005. C-di-GMP:The dawning of a novel bacterial signalling system. Mol. Microbiol. 57:629-39
84. Ross P, WeinhouseH,Aloni Y, Michaeli D, Weinberger-Ohana P, et al. 1987. Regulation of cellulose synthesis in Acetobacter xylinum by cyclic diguanylic acid. Nature 325:279-81
85. Ryan RP, Fouhy Y, Lucey JF, Crossman LC, Spiro S, et al. 2006a. Cell-cell signaling in Xanthomonas campestris involves an HD-GYP domain protein that functions in cyclic di-GMP turnover. Proc. Natl. Acad. Sci. USA 103:6712-17
86. Ryan RP, Fouhy Y, Lucey JF, Dow JM. 2006b. Cyclic di-GMP signaling in bacteria: recent advances and new puzzles. J. Bacteriol. 188:8327-34
87. Ryjenkov DA, Simm R, Romling U, Gomelsky M. 2006. The PilZ domain is a receptor for the second messenger c-di-GMP: The PilZ domain protein YcgR controls motility in enterobacteria. J. Biol. Chem. 281:30310-14
88. SauerK,CullenMC, Rickard AH, Zeef LA,Davies DG, Gilbert P. 2004. Characterization of nutrient-induced dispersion in Pseudomonas aeruginosa PAO1 biofilm. J. Bacteriol. 186:7312-26
89. SawaiH, Yoshioka S,UchidaT,Hyodo M, Hayakawa Y, et al. 2010. Molecular oxygen regulates the enzymatic activity of a heme-containing diguanylate cyclase (HemDGC) for the synthesis of cyclic di-GMP. Biochim. Biophys. Acta 1804:166-72
90. Schmidt AJ, Ryjenkov DA, Gomelsky M. 2005. The ubiquitous protein domain EAL is a cyclic diguanylatespecific phosphodiesterase: enzymatically active and inactive EAL domains. J. Bacteriol. 187:4774-81
91. Shin JS, Ryu KS, Ko J, Lee A, Choi BS. 2011. Structural characterization reveals that a PilZ domain protein undergoes substantial conformational change upon binding to cyclic dimeric guanosine monophosphate. Protein Sci. 20:270-77
92. Singh PK, Parsek MR, Greenberg EP,Welsh MJ. 2002. A component of innate immunity prevents bacterial biofilm development. Nature 417:552-55
93. Smith KD, Lipchock SV, Ames TD, Wang J, Breaker RR, Strobel SA. 2009. Structural basis of ligand binding by a c-di-GMP riboswitch. Nat. Struct. Mol. Biol. 16:1218-23
94. Smith KD, Shanahan CA, Moore EL, Simon AC, Strobel SA. 2011. Structural basis of differential ligand recognition by two classes of bis-(3-5)-cyclic dimeric guanosine monophosphate-binding riboswitches. Proc. Natl. Acad. Sci. USA 108:7757-62
95. Sowa Y, Berry RM. 2008. Bacterial flagellar motor. Q. Rev. Biophys. 41:103-32
96. Sudarsan N, Lee ER, Weinberg Z, Moy RH, Kim JN, et al. 2008. Riboswitches in eubacteria sense the second messenger cyclic di-GMP. Science 321:411-13
97. Tamayo R, Tischler AD, Camilli A. 2005. The EAL domain protein VieA is a cyclic diguanylate phosphodiesterase. J. Biol. Chem. 280:33324-30
98. Tao F, He YW, Wu DH, Swarup S, Zhang LH. 2010. The cyclic nucleotide monophosphate domain of Xanthomonas campestris global regulator Clp defines a new class of cyclic di-GMP effectors. J. Bacteriol. 192:1020-29
99. Tarutina M, Ryjenkov DA, Gomelsky M. 2006. An unorthodox bacteriophytochrome from Rhodobacter sphaeroides involved in turnover of the second messenger c-di-GMP. J. Biol. Chem. 281:34751-58
100. Taylor BL. 2007. Aer on the inside looking out: paradigm for a PAS-HAMP role in sensing oxygen, redox and energy. Mol. Microbiol. 65:1415-24
101. Terashima H, Kojima S, Homma M. 2008. Flagellar motility in bacteria structure and function of flagellar motor. Int. Rev. Cell Mol. Biol. 270:39-85
102. Thormann KM, Duttler S, Saville RM, Hyodo M, Shukla S, et al. 2006. Control of formation and cellular detachment from Shewanella oneidensis MR-1 biofilms by cyclic di-GMP. J. Bacteriol. 188:2681-91
103. Tischler AD, Camilli A. 2004. Cyclic diguanylate (c-di-GMP) regulates Vibrio cholerae biofilm formation. Mol. Microbiol. 53:857-69
104. Tuckerman JR, Gonzalez G, Gilles-Gonzalez MA. 2011. Cyclic di-GMP activation of polynucleotide phosphorylase signal-dependent RNA processing. J. Mol. Biol. 407:633-39
105. Tuckerman JR, Gonzalez G, Sousa EH, Wan X, Saito JA, et al. 2009. An oxygen-sensing diguanylate cyclase and phosphodiesterase couple for c-di-GMP control. Biochemistry 48:9764-74
106. Wan X, Tuckerman JR, Saito JA, Freitas TA, Newhouse JS, et al. 2009. Globins synthesize the second messenger bis-(3-5)-cyclic diguanosine monophosphate in bacteria. J. Mol. Biol. 388:262-70
107. Watnick PI, Fullner KJ, Kolter R. 1999. A role for the mannose-sensitive hemagglutinin in biofilm formation by Vibrio cholerae El Tor. J. Bacteriol. 181:3606-9
108. Weber H, Pesavento C, Possling A, Tischendorf G, Hengge R. 2006. Cyclic-di-GMP-mediated signaling within the sigma network of Escherichia coli. Mol. Microbiol. 62:1014-34
109. Weinhouse H, Sapir S, Amikam D, Shilo Y, Volman G, et al. 1997. c-di-GMP-binding protein, a new factor regulating cellulose synthesis in Acetobacter xylinum. FEBS Lett. 416:207-11
110. White BP. 1938. The rugose variant of Vibrios. J. Pathol. 46:1-6
111. Wilksch JJ, Yang J, Clements A, Gabbe JL, Short KR, et al. 2011. MrkH, a novel c-di-GMP-dependent transcriptional activator, controls Klebsiella pneumoniae biofilm formation by regulating type 3 fimbriae expression. PLoS Pathog. 7:e1002204
112. Williams SB, Stewart V. 1999. Functional similarities among two-component sensors and methyl-accepting chemotaxis proteins suggest a role for linker region amphipathic helices in transmembrane signal transduction. Mol. Microbiol. 33:1093-102
113. Wolfe AJ, Visick KL. 2008. Get the message out: cyclic-di-GMP regulates multiple levels of flagellum-based motility. J. Bacteriol. 190:463-75
114. Yildiz FH, Schoolnik GK. 1999. 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 96:4028-33
115. Zakikhany K, Harrington CR, Nimtz M, Hinton JC, Romling U. 2010. Unphosphorylated CsgD controls biofilm formation in Salmonella enterica serovar Typhimurium. Mol. Microbiol. 77:771-86
116. Zhou J, Lloyd SA, Blair DF. 1998. Electrostatic interactions between rotor and stator in the bacterial flagellar motor. Proc. Natl. Acad. Sci. USA 95:6436-41