Skip to main content
SpringerLink
Log in

Structure and Regulation of EAL Domain Proteins

  • Chapter
  • First Online:
Microbial Cyclic Di-Nucleotide Signaling

  • 906 Accesses

Abstract

The formation and dispersal of bacterial biofilms is strongly correlated with cellular levels of bis-(3′–5′) cyclic dimeric guanosine monophosphate, cyclic di-GMP, a secondary messenger that has been shown to be involved in regulation of a broad range of cellular processes in bacteria. Diguanylate cyclases (DGCs) are required for synthesis of cyclic di-GMP, with phosphodiesterases (PDEs) responsible for its breakdown. This review focuses on PDEs characterised by the presence of the conserved “EAL” sequence motif. Typically found in multi-domain proteins, EAL domains can couple to sensory or regulatory domains that allow their activity to be regulated by environmental stimuli or cellular cues. Additionally, catalytically inactive EAL PDEs are suggested to have a sensory or otherwise regulatory function. Recent structure determination provides a wealth of information on PDE function and regulation and has provided novel insight into the enzymatic reaction mechanism. Several regulatory layers may control activity, including dimerisation, active site formation, and metal coordination. In this review, we provide a concise summary of these exciting findings and highlight open research questions that will allow us in future to decipher many of the cellular signals responsible for regulation of PDE activity and cellular processes influenced by these pivotal enzymes.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 109.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 139.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 219.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  1. Leewenhoeck A (1683) An abstract of a letter from Mr. Anthony Leevvenhoeck at Delft, dated Sep. 17. 1683. Containing some microscopical observations, about animals in the scurf of the teeth, the substance call’d worms in the nose, the cuticula consisting of scales. Philos Trans R Soc Lond 14

    Google Scholar 

  2. Hoiby N, Axelsen NH (1973) Identification and quantitation of precipitins against Pseudomonas aeruginosa in patients with cystic fibrosis by means of crossed immunoelectrophoresis with intermediate gel. Acta Pathol Microbiol Scand B: Microbiol Immunol 81:298–308

    CAS  Google Scholar 

  3. Neu TR, Lawrence JR (2009) Extracellular polymeric substances in microbial biofilms. In: Moran A, Holst O, Brennan P, von Itzstein M (eds) Microbial glycobiology: Structures, relevance and applications. Academic Press, Cambridge, pp 735–758

    Google Scholar 

  4. Stoodley P, Sauer K, Davies DG, Costerton JW (2002) Biofilms as complex differentiated communities. Annu Rev Microbiol 56:187–209

    Article  CAS  PubMed  Google Scholar 

  5. Moser C et al (2017) Biofilms and host response – helpful or harmful. APMIS 125:320–338

    Article  PubMed  Google Scholar 

  6. Costerton JW, Stewart PS, Greenberg EP (1999) Bacterial biofilms: a common cause of persistent infections. Science 284:1318–1322

    Article  CAS  PubMed  Google Scholar 

  7. Shirtliff ME, Leid JG (2009) The role of biofilms in device-related infections. Springer, Berlin

    Book  Google Scholar 

  8. Boles BR, McCarter LL (2002) Vibrio parahaemolyticus scrABC, a novel operon affecting swarming and capsular polysaccharide regulation. J Bacteriol 184:5946–5954

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. D’Argenio DA, Calfee MW, Rainey PB, Pesci EC (2002) Autolysis and autoaggregation in Pseudomonas aeruginosa colony morphology mutants. J Bacteriol 184:6481–6489

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  10. Simm R, Morr M, Kader A, Nimtz M, Römling U (2004) GGDEF and EAL domains inversely regulate cyclic di-GMP levels and transition from sessility to motility. Mol Microbiol 53:1123–1134

    Article  CAS  PubMed  Google Scholar 

  11. Tischler AD, Camilli A (2004) Cyclic diguanylate (c-di-GMP) regulates Vibrio cholerae biofilm formation. Mol Microbiol 53:857–869

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Römling U, Galperin MY, Gomelsky M (2013) Cyclic di-GMP: the first 25 years of a universal bacterial second messenger. Microbiol Mol Biol Rev 77:1–52

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  13. Jenal U, Reinders A, Lori C (2017) Cyclic di-GMP: second messenger extraordinaire. Nat Rev Microbiol 15:271–284

    Article  CAS  PubMed  Google Scholar 

  14. Römling U, Liang ZX, Dow JM (2017) Progress in understanding the molecular basis underlying functional diversification of cyclic dinucleotide turnover proteins. J Bacteriol 199:e00790-16

    Article  PubMed  PubMed Central  Google Scholar 

  15. Deepthi A, Liew CW, Liang ZX, Swaminathan K, Lescar J (2014) Structure of a diguanylate cyclase from Thermotoga maritima: Insights into activation, feedback inhibition and thermostability. PLoS One 9:1–9

    Article  CAS  Google Scholar 

  16. Tchigvintsev A et al (2010) Structural insight into the mechanism of c-di-GMP hydrolysis by EAL domain phosphodiesterases. J Mol Biol 402:524–538

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Bellini D et al (2014) Crystal structure of an HD-GYP domain cyclic-di-GMP phosphodiesterase reveals an enzyme with a novel trinuclear catalytic iron centre. Mol Microbiol 91:26–38

    Article  CAS  PubMed  Google Scholar 

  18. Ross P, Weinhouse H, Aloni Y (1987) Regulation of cellulose synthesis in Acetobacter xylinum by cyclic diguanylic acid. Nature 325:279–281

    Article  CAS  PubMed  Google Scholar 

  19. Römling U, Gomelsky M, Galperin MY (2005) C-di-GMP: the dawning of a novel bacterial signalling system. Mol Microbiol 57:629–639

    Article  CAS  PubMed  Google Scholar 

  20. Wolfe AJ, Visick KL (2008) Get the message out: Cyclic-Di-GMP regulates multiple levels of flagellum-based motility. J Bacteriol 190:463–475

    Article  CAS  PubMed  Google Scholar 

  21. Hengge R (2009) Principles of c-di-GMP signalling in bacteria. Nat Rev Microbiol 7:263–273

    Article  CAS  PubMed  Google Scholar 

  22. Chan C et al (2004) Structural basis of activity and allosteric control of diguanylate cyclase. Proc Natl Acad Sci USA 101:17084–17089

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Paul R et al (2004) Cell cycle-dependent dynamic localization of a bacterial response regulator with a novel di-guanylate cyclase output domain. Genes Dev 18:715–727

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Ryjenkov DA, Tarutina M, Moskvin OV, Gomelsky M (2005) Cyclic diguanylate is a ubiquitous signaling molecule in bacteria: insights into biochemistry of the GGDEF protein domain. J Bacteriol 187:1792–1798

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Schirmer T (2016) C-di-GMP synthesis: structural aspects of evolution, catalysis and regulation. J Mol Biol 428:3683–3701

    Article  CAS  PubMed  Google Scholar 

  26. Sauer K et al (2004) Characterization of nutrient-induced dispersion in Pseudomonas aeruginosa PAO1 biofilm. J Bacteriol 186:7312–7326

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Thormann KM et al (2006) Control of formation and cellular detachment from Shewanella oneidensis MR-1 biofilms by cyclic di-GMP. J Bacteriol 188:2681–2691

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Schmidt AJ, Ryjenkov DA, Gomelsky M (2005) The ubiquitous protein domain EAL is a cyclic diguanylate-specific phosphodiesterase: enzymatically active and inactive EAL domains. J Bacteriol 187:4774–4781

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Tamayo R, Tischler AD, Camilli A (2005) The EAL domain protein VieA is a cyclic diguanylate phosphodiesterase. J Biol Chem 280:33324–33330

    Article  CAS  PubMed  Google Scholar 

  30. Stelitano V et al (2013) C-di-GMP hydrolysis by Pseudomonas aeruginosa HD-GYP phosphodiesterases: analysis of the reaction mechanism and novel roles for pGpG. PLoS One 8:e74920

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Miner KD, Klose KE, Kurtz DM Jr (2013) An HD-GYP cyclic di-guanosine monophosphate phosphodiesterase with a non-heme diiron-carboxylate active site. Biochemistry 52:5329–5331

    Article  CAS  PubMed  Google Scholar 

  32. 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 280:30829–30837

    Article  CAS  PubMed  Google Scholar 

  33. Kulasakara H et al (2006) Analysis of Pseudomonas aeruginosa diguanylate cyclases and phosphodiesterases reveals a role for bis-(3′–5′)-cyclic-GMP in virulence. Proc Natl Acad Sci USA 103:2839–2844

    Article  CAS  PubMed  Google Scholar 

  34. 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 281:34751–34758

    Article  CAS  PubMed  Google Scholar 

  35. Phippen CW et al (2014) Formation and dimerization of the phosphodiesterase active site of the Pseudomonas aeruginosa MorA, a bi-functional c-di-GMP regulator. FEBS Lett 588:4631–4636

    Article  CAS  PubMed  Google Scholar 

  36. Sundriyal A et al (2014) Inherent regulation of EAL domain-catalyzed hydrolysis of second messenger cyclic di-GMP. J Biol Chem 289:6978–6990

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Valentini M, Filloux A (2016) Biofilms and c-di-GMP signaling: lessons from Pseudomonas aeruginosa and other bacteria. J Biol Chem 291:12547–12555

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Cohen D et al (2015) Oligoribonuclease is a central feature of cyclic diguanylate signaling in Pseudomonas aeruginosa. Proc Natl Acad Sci 112(36):11359–11364

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Lacey MM, Partridge JD, Green J (2010) Escherichia coli K-12 YfgF is an anaerobic cyclic di-GMP phosphodiesterase with roles in cell surface remodelling and the oxidative stress response. Microbiology 156:2873–2886

    Article  CAS  PubMed  Google Scholar 

  40. Orr MW et al (2015) Oligoribonuclease is the primary degradative enzyme for pGpG in Pseudomonas aeruginosa that is required for cyclic-di-GMP turnover. Proc Natl Acad Sci 112(36):E5048–E5057

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Orr MW et al (2018) A subset of exoribonucleases serve as degradative enzymes for pGpG in c-di-GMP signaling. J Bacteriol 200:e00300–e00318

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Tal R et al (1998) Three cdg operons control cellular turnover of cyclic di-GMP in Acetobacter xylinum: genetic organization and occurrence of conserved domains in isoenzymes. J Bacteriol 180:4416–4425

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Bobrov AG, Kirillina O, Perry RD (2005) The phosphodiesterase activity of the HmsP EAL domain is required for negative regulation of biofilm formation in Yersinia pestis. FEMS Microbiol Lett 247:123–130

    Article  CAS  PubMed  Google Scholar 

  44. Rao F, Yang Y, Qi Y, Liang Z-X (2008) Catalytic mechanism of cyclic di-GMP-specific phosphodiesterase: a study of the EAL domain-containing RocR from Pseudomonas aeruginosa. J Bacteriol 190:3622–3631

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Barends TRM et al (2009) Structure and mechanism of a bacterial light-regulated cyclic nucleotide phosphodiesterase. Nature 459:1015–1018

    Article  CAS  PubMed  Google Scholar 

  46. Tarnawski M, Barends TRM, Hartmann E, Schlichting I (2013) Structures of the catalytic EAL domain of the Escherichia coli direct oxygen sensor. Acta Crystallogr D Biol Crystallogr 69:1045–1053

    Article  CAS  PubMed  Google Scholar 

  47. Winkler A et al (2014) Characterization of elements involved in allosteric light regulation of phosphodiesterase activity by comparison of different functional BlrP1 states. J Mol Biol 426:853–868

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Rao F et al (2009) The functional role of a conserved loop in EAL domain-based cyclic di-GMP-specific phosphodiesterase. J Bacteriol 191:4722–4731

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Römling U (2009) Rationalizing the evolution of EAL domain-based cyclic di-GMP-specific phosphodiesterases. J Bacteriol 191:4697–4700

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  50. Minasov G et al (2009) Crystal structures of YkuI and its complex with second messenger cyclic di-GMP suggest catalytic mechanism of phosphodiester bond cleavage by EAL domains. J Biol Chem 284:13174–13184

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. 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 393:848–866

    Article  CAS  PubMed  Google Scholar 

  52. Rao F et al (2009) Enzymatic synthesis of c-di-GMP using a thermophilic diguanylate cyclase. Anal Biochem 389:138–142

    Article  CAS  PubMed  Google Scholar 

  53. Berman HM, Westbrook J, Feng Z, Gilliland G, Bhat TN, Weissig H, Shindyalov IN, Bourne PE (2000) The Protein Data Bank. Nucleic Acids Research 28:235–242

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Navarro MVAS, De N, Bae N, Wang Q, Sondermann H (2009) Structural analysis of the GGDEF-EAL domain-containing c-di-GMP receptor FimX. Structure 17:1104–1116

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Huang ZJ, Edery I, Rosbash M (1993) PAS is a dimerization domain common to Drosophila period and several transcription factors. Nature 364:259–262

    Article  CAS  PubMed  Google Scholar 

  56. Iseki M et al (2002) A blue-light-activated adenylyl cyclase mediates photoavoidance in Euglena gracilis. Nature 415:1047–1051

    Article  CAS  PubMed  Google Scholar 

  57. Masuda S, Bauer CE (2002) AppA is a blue light photoreceptor that antirepresses photosynthesis gene expression in Rhodobacter sphaeroides. Cell 110:613–623

    Article  CAS  PubMed  Google Scholar 

  58. Huang B, Whitchurch CB, Mattick JS (2003) FimX, a multidomain protein connecting environmental signals to twitching motility in Pseudomonas aeruginosa. J Bacteriol 185:7068–7076

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. Kazmierczak BI, Lebron MB, Murray TS (2006) Analysis of FimX, a phosphodiesterase that governs twitching motility in Pseudomonas aeruginosa. Mol Microbiol 60:1026–1043

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Guzzo CR, Dunger G, Salinas RK, Farah CS (2013) Structure of the PilZ-FimXEAL-c-di-GMP complex responsible for the regulation of bacterial type IV pilus biogenesis. J Mol Biol 425:2174–2197

    Article  CAS  PubMed  Google Scholar 

  61. Xiong Y, Lu HT, Li Y, Yang GF, Zhan CG (2006) Characterization of a catalytic ligand bridging metal ions in phosphodiesterases 4 and 5 by molecular dynamics simulations and hybrid quantum mechanical/molecular mechanical calculations. Biophys J 91:1858–1867

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. Salter EA, Wierzbicki A (2007) The mechanism of cyclic nucleotide hydrolysis in the phosphodiesterase catalytic site. J Phys Chem B 111:4547–4552

    Article  CAS  PubMed  Google Scholar 

  63. Galperin MY, Nikolskaya AN, Koonin EV (2001) Novel domains of the prokaryotic two-component signal transduction systems. FEMS Microbiol Lett 203:11–21

    Article  CAS  PubMed  Google Scholar 

  64. Chang F-Y, Lu CL, Peng H-L (2004) Evolutionary analysis of the two-component systems in Pseudomonas aeruginosa PAO1. J Mol Evol 59:725–737

    Article  PubMed  CAS  Google Scholar 

  65. Galperin MY (2010) Diversity of structure and function of response regulator output domains. Curr Opin Microbiol 13:150–159

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. Navarro MVAS et al (2011) Structural basis for c-di-GMP-mediated inside-out signaling controlling periplasmic proteolysis. PLoS Biol 9:e1000588

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  67. Chen MW et al (2012) Structural insights into the regulatory mechanism of the response regulator RocR from Pseudomonas aeruginosa in cyclic di-GMP signaling. J Bacteriol 194:4837–4846

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  68. Newell PD, Monds RD, O’Toole GA (2009) LapD is a bis-(3′,5′)-cyclic dimer GMP-binding protein that regulates surface attachment by Pseudomonas fluorescens Pf0–1. Proc Natl Acad Sci USA 106:3461–3466

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  69. Newell PD, Boyd CD, Sondermann H, O’Toole GA (2011) A c-di-GMP effector system controls cell adhesion by inside-out signaling and surface protein cleavage. PLoS Biol 9:e1000587

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  70. Liu C et al (2018) Insights into biofilm dispersal regulation from the crystal structure of the PAS-GGDEF-EAL region of RbdA from Pseudomonas aeruginosa. J Bacteriol 200:e00515-17

    Article  PubMed  PubMed Central  Google Scholar 

  71. Mantoni F et al (2018) Insights into the GTP-dependent allosteric control of c-di-GMP hydrolysis from the crystal structure of PA0575 protein from Pseudomonas aeruginosa. FEBS J 285:3815–3834

    Article  CAS  PubMed  Google Scholar 

  72. Bellini D et al (2017) Dimerisation induced formation of the active site and the identification of three metal sites in EAL-phosphodiesterases. Sci Rep 7:42166–42166

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  73. Hay ID, Remminghorst U, Rehm BH a (2009) MucR, a novel membrane-associated regulator of alginate biosynthesis in Pseudomonas aeruginosa. Appl Environ Microbiol 75:1110–1120

    Article  CAS  PubMed  Google Scholar 

  74. Li Y, Heine S, Entian M, Sauer K, Frankenberg-Dinkel N (2013) NO-induced biofilm dispersion in Pseudomonas aeruginosa is mediated by an MHYT domain-coupled phosphodiesterase. J Bacteriol 195:3531–3542

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  75. Wang Y, Hay ID, Rehman ZU, Rehm BH a (2015) Membrane-anchored MucR mediates nitrate-dependent regulation of alginate production in Pseudomonas aeruginosa. Appl Microbiol Biotechnol 99:7253–7265

    Article  CAS  PubMed  Google Scholar 

  76. Miner KD, Kurtz DM (2016) Active site metal occupancy and cyclic di-GMP phosphodiesterase activity of Thermotoga maritima HD-GYP. Biochemistry 55:970–979

    Article  CAS  PubMed  Google Scholar 

  77. Syson K et al (2008) Three metal ions participate in the reaction catalyzed by T5 flap endonuclease. J Biol Chem 283:28741–28746

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  78. Kim Y et al (1995) Crystal structure of Thermus aquaticus DNA polymerase. Nature 376:612–616

    Article  CAS  PubMed  Google Scholar 

  79. Prasannan CB, Xie F, Dupureur CM (2010) Characterizing metalloendonuclease mixed metal complexes by global kinetic analysis. J Biol Inorg Chem 15:533–545

    Article  CAS  PubMed  Google Scholar 

  80. Robert-Paganin J, Nonin-Lecomte S, Réty S (2012) Crystal structure of an EAL domain in complex with reaction product 5′-pGpG. PLoS One 7:e52424–e52424

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  81. Qi Y et al (2011) Binding of cyclic diguanylate in the non-catalytic EAL domain of FimX induces a long-range conformational change. J Biol Chem 286:2910–2917

    Article  CAS  PubMed  Google Scholar 

  82. 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

    Article  CAS  PubMed  Google Scholar 

  83. Wei Q, Ma LZ (2013) Biofilm matrix and its regulation in Pseudomonas aeruginosa. Int J Mol Sci 14:20983–21005

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  84. Barraud N et al (2006) Involvement of nitric oxide in biofilm dispersal of Pseudomonas aeruginosa. J Bacteriol 188:7344–7353

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  85. Howlin RP et al (2017) Low-dose nitric oxide as targeted anti-biofilm adjunctive therapy to treat chronic Pseudomonas aeruginosa infection in cystic fibrosis. Mol Ther 25:2104–2116

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  86. Barraud N et al (2012) Cephalosporin-3′-diazeniumdiolates: targeted NO-donor prodrugs for dispersing bacterial biofilms. Angew Chem Int Ed Engl 51:9057–9060

    Article  CAS  PubMed  Google Scholar 

  87. Barraud N, Kelso MJ, Rice SA, Kjelleberg S (2015) Nitric oxide: a key mediator of biofilm dispersal with applications in infectious diseases. Curr Pharm Des 21:31–42

    Article  CAS  PubMed  Google Scholar 

  88. Collins SA et al (2017) Cephalosporing-3′-diazeniumdiolate NO donor prodrug PYRRO-C3D enhances azithromycin susceptibility of nontypeable Haemophilus influenzae biofilms. Antimicrob Agents Chemother 61:1–12

    Google Scholar 

  89. Liu N et al (2012) Nitric oxide regulation of cyclic di-GMP synthesis and hydrolysis in Shewanella woodyi. Biochemistry 51:2087–2099

    Article  CAS  PubMed  Google Scholar 

  90. Hossain S, Boon EM (2017) Discovery of a novel nitric oxide binding protein and nitric-oxide-responsive signaling pathway in Pseudomonas aeruginosa. ACS Infect Dis 3(6):454–461

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  91. Bacon B, Liu Y, Kincaid JR, Boon EM (2018) Spectral characterization of a novel NO sensing protein in bacteria: NosP. Biochemistry 57:6187–6200

    Article  CAS  PubMed  Google Scholar 

  92. Hossain S, Nisbett LM, Boon EM (2017) Discovery of two bacterial nitric oxide-responsive proteins and their roles in bacterial biofilm regulation. Acc Chem Res 50:1633–1639

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  93. Barraud N et al (2009) Nitric oxide signaling in Pseudomonas aeruginosa biofilms mediates phosphodiesterase activity, decreased cyclic di-GMP levels, and enhanced dispersal. J Bacteriol 191:7333–7342

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  94. Roy AB, Petrova OE, Sauer K (2012) The phosphodiesterase DipA (PA5017) is essential for Pseudomonas aeruginosa biofilm dispersion. J Bacteriol 194:2904–2915

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  95. Galperin MY, Gaidenko T, Mulkidjanian AY, Nakano M, Price CW (2001) MHYT, a new integral membrane sensor domain. FEMS Microbiol Lett 205:17–23

    Article  CAS  PubMed  Google Scholar 

  96. Cutruzzola F, Frankenberg-Dinkel N (2015) Origin and impact of nitric oxide in Pseudomonas aeruginosa biofilms. J Bacteriol 198:55–65

    Article  PubMed Central  CAS  Google Scholar 

  97. Grimes JM et al (2018) Where is crystallography going? Acta Cryst Sect D Struct Biol 74:152–166

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. School of Life Sciences, University of Warwick, Coventry, UK

    Dom Bellini

  2. Research Complex at Harwell, Harwell Science and Innovation Campus, Didcot, Oxfordshire, UK

    Dom Bellini & Martin A. Walsh

  3. Structure and Function of Biological Membranes Lab, Université Libre de Bruxelles, Bruxelles, Belgium

    Andrew Hutchin

  4. Biological Sciences, University of Southampton, Southampton, UK

    Odel Soren, Jeremy S. Webb & Ivo Tews

  5. Diamond Light Source, Harwell Science and Innovation Campus, Didcot, Oxfordshire, UK

    Martin A. Walsh

Authors
  1. Dom Bellini
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Andrew Hutchin
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Odel Soren
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Jeremy S. Webb
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Ivo Tews
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Martin A. Walsh
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Martin A. Walsh .

Editor information

Editors and Affiliations

  1. Institute of Biochemistry and Agricultural Biotechnology Center, National Chung Hsing University, Taichung, Taiwan

    Shan-Ho Chou

  2. Department of Biology, Faculty of Sciences, Universidad de Chile, Santiago, Chile

    Nicolas Guiliani

  3. Department of Cell Biology and Molecular Genetics, University of Maryland, College Park, MD, USA

    Vincent T. Lee

  4. Department of Microbiology, Tumor and Cell Biology, Karolinska Institutet, Stockholm, Sweden

    Ute Römling

Rights and permissions

Reprints and permissions

Copyright information

© 2020 Springer Nature Switzerland AG

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Bellini, D., Hutchin, A., Soren, O., Webb, J.S., Tews, I., Walsh, M.A. (2020). Structure and Regulation of EAL Domain Proteins. In: Chou, SH., Guiliani, N., Lee, V., Römling, U. (eds) Microbial Cyclic Di-Nucleotide Signaling. Springer, Cham. https://doi.org/10.1007/978-3-030-33308-9_2

Download citation

Publish with us

Policies and ethics

Search

Navigation