Skip to main content
SpringerLink
Log in

Sensory Domains That Control Cyclic di-GMP-Modulating Proteins: A Critical Frontier in Bacterial Signal Transduction

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

Abstract

Sensory domain-containing proteins that modulate levels of the intracellular second messenger cyclic diguanylate (cyclic di-GMP) have the potential to form direct regulatory links between local conditions and bacterial behaviors. Coupling the detection of external stimuli (e.g. O2, small molecule signals, or light) to the control of cyclic di-GMP-regulated activities such as swimming and matrix production allows bacteria to adapt immediately to environmental changes. Much of this coupling is mediated by Per-Arnt-Sim (PAS) domains, which are found throughout the tree of life and can bind diverse cofactors and ligands. Here, we describe selected proteins with both sensory domains and those involved in cyclic di-GMP synthesis or degradation that has been studied in diverse bacteria, focusing on PAS domains and highlighting the stimulus perception mechanisms that enable their physiological roles. We also provide an overview of the sets of proteins with both PAS and cyclic di-GMP-modulating domains in Escherichia coli and Pseudomonas aeruginosa and use structure-based modeling to predict the sensory capabilities of those that have not been characterized. More detailed models of environmental sensing and intracellular signaling will facilitate efforts to control bacterial activities in various contexts.

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. 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 

  2. 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 

  3. 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 

  4. Flemming H-C, Wingender J, Szewzyk U et al (2016) Biofilms: an emergent form of bacterial life. Nat Rev Microbiol 14:563–575

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  6. Ha D-G, O’Toole GA (2015) c-di-GMP and its effects on biofilm formation and dispersion: a Pseudomonas aeruginosa review. Microbiol Spectr 3:MB-0003-2014

    PubMed  Google Scholar 

  7. Römling U, Galperin MY (2017) Discovery of the second messenger cyclic di-GMP. Methods Mol Biol 1657:1–8

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  8. Mulder NJ, Apweiler R, Attwood TK et al (2002) InterPro: an integrated documentation resource for protein families, domains and functional sites. Brief Bioinform 3:225–235

    Article  CAS  PubMed  Google Scholar 

  9. Möglich A, Ayers RA, Moffat K (2009) Structure and signaling mechanism of Per-ARNT-Sim domains. Structure 17:1282–1294

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  10. Galperin MY (2004) Bacterial signal transduction network in a genomic perspective. Environ Microbiol 6:552–567

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Freitas TAK, Saito JA, Wan X et al (2008) Chapter 7 – Protoglobin and globin-coupled sensors. In: Ghosh A (ed) The smallest biomolecules: diatomics and their interactions with heme proteins. Elsevier, Amsterdam, pp 175–202

    Chapter  Google Scholar 

  12. Anantharaman V, Aravind L (2001) The CHASE domain: a predicted ligand-binding module in plant cytokinin receptors and other eukaryotic and bacterial receptors. Trends Biochem Sci 26:579–582

    Article  CAS  PubMed  Google Scholar 

  13. Herbst S, Lorkowski M, Sarenko O et al (2018) Transmembrane redox control and proteolysis of PdeC, a novel type of c-di-GMP phosphodiesterase. EMBO J 37:e97825. https://doi.org/10.15252/embj.201797825

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Henry JT, Crosson S (2011) Ligand-binding PAS domains in a genomic, cellular, and structural context. Annu Rev Microbiol 65:261–286

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Finn RD, Mistry J, Schuster-Böckler B et al (2006) Pfam: clans, web tools and services. Nucleic Acids Res 34:D247–D251

    Article  CAS  PubMed  Google Scholar 

  16. Letunic I, Bork P (2018) 20 years of the SMART protein domain annotation resource. Nucleic Acids Res 46:D493–D496

    Article  CAS  PubMed  Google Scholar 

  17. Römling U, Balsalobre C (2012) Biofilm infections, their resilience to therapy and innovative treatment strategies. J Intern Med 272:541–561

    Article  PubMed  CAS  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  19. Tal R, Wong HC, Calhoon 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 

  20. Chang AL, Tuckerman JR, Gonzalez G et al (2001) Phosphodiesterase A1, a regulator of cellulose synthesis in Acetobacter xylinum, is a heme-based sensor. Biochemistry 40:3420–3426

    Article  CAS  PubMed  Google Scholar 

  21. Qi Y, Rao F, Luo Z, Liang Z-X (2009) A flavin cofactor-binding PAS domain regulates c-di-GMP synthesis in AxDGC2 from Acetobacter xylinum. Biochemistry 48:10275–10285

    Article  CAS  PubMed  Google Scholar 

  22. Delgado-Nixon VM, Gonzalez G, Gilles-Gonzalez MA (2000) Dos, a heme-binding PAS protein from Escherichia coli, is a direct oxygen sensor. Biochemistry 39:2685–2691

    Article  CAS  PubMed  Google Scholar 

  23. Tuckerman JR, Gonzalez G, Sousa EHS et al (2009) An oxygen-sensing diguanylate cyclase and phosphodiesterase couple for c-di-GMP control. Biochemistry 48:9764–9774

    Article  CAS  PubMed  Google Scholar 

  24. Sarenko O, Klauck G, Wilke FM et al (2017) More than enzymes that make or break cyclic di-GMP-local signaling in the interactome of GGDEF/EAL domain proteins of Escherichia coli. MBio 8:e01639-17. https://doi.org/10.1128/mBio.01639-17

    Article  PubMed  PubMed Central  Google Scholar 

  25. Tagliabue A, Bopp L, Dutay J-C et al (2010) Hydrothermal contribution to the oceanic dissolved iron inventory. Nat Geosci 3:252

    Article  CAS  Google Scholar 

  26. Donné J, Van Kerckhoven M, Maes L et al (2016) The role of the globin-coupled sensor YddV in a mature E. coli biofilm population. Biochim Biophys Acta 1864:835–839

    Article  PubMed  CAS  Google Scholar 

  27. Tuckerman JR, Gonzalez G, Gilles-Gonzalez M-A (2011) Cyclic di-GMP activation of polynucleotide phosphorylase signal-dependent RNA processing. J Mol Biol 407:633–639

    Article  CAS  PubMed  Google Scholar 

  28. Kwan BW, Osbourne DO, Hu Y et al (2015) Phosphodiesterase DosP increases persistence by reducing cAMP which reduces the signal indole. Biotechnol Bioeng 112:588–600

    Article  CAS  PubMed  Google Scholar 

  29. Friedman L, Kolter R (2004) Genes involved in matrix formation in Pseudomonas aeruginosa PA14 biofilms. Mol Microbiol 51:675–690

    Article  CAS  PubMed  Google Scholar 

  30. Jo J, Cortez KL, Cornell WC et al (2017) An orphan cbb3-type cytochrome oxidase subunit supports Pseudomonas aeruginosa biofilm growth and virulence. eLife 6:e30205

    Google Scholar 

  31. Xu KD, Stewart PS, Xia F et al (1998) Spatial physiological heterogeneity in Pseudomonas aeruginosa biofilm is determined by oxygen availability. Appl Environ Microbiol 64:4035–4039

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Dietrich LEP, Okegbe C, Price-Whelan A et al (2013) Bacterial community morphogenesis is intimately linked to the intracellular redox state. J Bacteriol 195:1371–1380

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Wang Y, Kern SE, Newman DK (2010) Endogenous phenazine antibiotics promote anaerobic survival of Pseudomonas aeruginosa via extracellular electron transfer. J Bacteriol 192:365–369

    Article  CAS  PubMed  Google Scholar 

  34. Dietrich LEP, Teal TK, Price-Whelan A, Newman DK (2008) Redox-active antibiotics control gene expression and community behavior in divergent bacteria. Science 321:1203–1206

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Lin Y-C, Sekedat MD, Cornell WC et al (2018) Phenazines regulate Nap-dependent denitrification in Pseudomonas aeruginosa biofilms. J Bacteriol 200(9):e00031-18. https://doi.org/10.1128/JB.00031-18

    Article  PubMed  PubMed Central  Google Scholar 

  36. Madsen JS, Lin Y-C, Squyres GR et al (2015) Facultative control of matrix production optimizes competitive fitness in Pseudomonas aeruginosa PA14 biofilm models. Appl Environ Microbiol 81:8414–8426

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Okegbe C, Fields BL, Cole SJ et al (2017) Electron-shuttling antibiotics structure bacterial communities by modulating cellular levels of c-di-GMP. Proc Natl Acad Sci USA 114:E5236–E5245

    CAS  PubMed  PubMed Central  Google Scholar 

  38. Li Y, Xia H, Bai F et al (2007) Identification of a new gene PA5017 involved in flagella-mediated motility, chemotaxis and biofilm formation in Pseudomonas aeruginosa. FEMS Microbiol Lett 272:188–195

    Article  CAS  PubMed  Google Scholar 

  39. Laventie B-J, Sangermani M, Estermann F et al (2019) A surface-induced asymmetric program promotes tissue colonization by Pseudomonas aeruginosa. Cell Host Microbe 25:140–152.e6

    Article  CAS  PubMed  Google Scholar 

  40. 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 

  41. Kulasekara BR, Kamischke C, Kulasekara HD et al (2013) c-di-GMP heterogeneity is generated by the chemotaxis machinery to regulate flagellar motility. eLife 2:e01402

    Google Scholar 

  42. Almblad H, Randall TE, Rich JD, et al (2019, submitted) Bacterial cyclic diguanylate signaling networks sense temperature

    Google Scholar 

  43. Elias M, Wieczorek G, Rosenne S, Tawfik DS (2014) The universality of enzymatic rate-temperature dependency. Trends Biochem Sci 39:1–7

    Article  CAS  PubMed  Google Scholar 

  44. Dhaka A, Viswanath V, Patapoutian A (2006) Trp ion channels and temperature sensation. Annu Rev Neurosci 29:135–161

    Article  CAS  PubMed  Google Scholar 

  45. Vriens J, Nilius B, Voets T (2014) Peripheral thermosensation in mammals. Nat Rev Neurosci 15:573–589

    Article  CAS  PubMed  Google Scholar 

  46. Kang K, Panzano VC, Chang EC et al (2011) Modulation of TRPA1 thermal sensitivity enables sensory discrimination in Drosophila. Nature 481:76–80

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  47. Deng Y, Schmid N, Wang C et al (2012) Cis-2-dodecenoic acid receptor RpfR links quorum-sensing signal perception with regulation of virulence through cyclic dimeric guanosine monophosphate turnover. Proc Natl Acad Sci USA 109:15479–15484

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Fazli M, Almblad H, Rybtke ML et al (2014) Regulation of biofilm formation in Pseudomonas and Burkholderia species. Environ Microbiol 16:1961–1981

    Article  CAS  PubMed  Google Scholar 

  49. Schmid N, Suppiger A, Steiner E et al (2017) High intracellular c-di-GMP levels antagonize quorum sensing and virulence gene expression in Burkholderia cenocepacia H111. Microbiology 163:754–764

    Article  CAS  PubMed  Google Scholar 

  50. Waldron EJ, Snyder D, Fernandez NL et al (2019) Structural basis of DSF recognition by its receptor RpfR and its regulatory interaction with the DSF synthase RpfF. PLoS Biol 17:e3000123

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Enomoto G, Nomura R, Shimada T et al (2014) Cyanobacteriochrome SesA is a diguanylate cyclase that induces cell aggregation in Thermosynechococcus. J Biol Chem 289:24801–24809

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Enomoto G, Ni-Ni-Win, Narikawa R, Ikeuchi M (2015) Three cyanobacteriochromes work together to form a light color-sensitive input system for c-di-GMP signaling of cell aggregation. Proc Natl Acad Sci USA 112(26):8082–8087

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Zavafer A, Cheah MH, Hillier W et al (2015) Photodamage to the oxygen evolving complex of photosystem II by visible light. Sci Rep 5:16363

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Schirmer T, Jenal U (2009) Structural and mechanistic determinants of c-di-GMP signalling. Nat Rev Microbiol 7:724–735

    Article  CAS  PubMed  Google Scholar 

  55. Al-Bassam MM, Haist J, Neumann SA et al (2018) Expression patterns, genomic conservation and input into developmental regulation of the GGDEF/EAL/HD-GYP domain proteins in Streptomyces. Front Microbiol 9:2524

    Article  PubMed  PubMed Central  Google Scholar 

  56. Dahlstrom KM, Collins AJ, Doing G et al (2018) A multimodal strategy used by a large c-di-GMP network. J Bacteriol 200:e00703-17. https://doi.org/10.1128/JB.00703-17

    Article  PubMed  PubMed Central  Google Scholar 

  57. Gilles-Gonzalez MA, Gonzalez G, Perutz MF et al (1994) Heme-based sensors, exemplified by the kinase FixL, are a new class of heme protein with distinctive ligand binding and autoxidation. Biochemistry 33:8067–8073

    Article  CAS  PubMed  Google Scholar 

  58. Purcell EB, McDonald CA, Palfey BA, Crosson S (2010) An analysis of the solution structure and signaling mechanism of LovK, a sensor histidine kinase integrating light and redox signals. Biochemistry 49:6761–6770

    Article  CAS  PubMed  Google Scholar 

  59. Ukaegbu UE, Henery S, Rosenzweig AC (2006) Biochemical characterization of MmoS, a sensor protein involved in copper-dependent regulation of soluble methane monooxygenase. Biochemistry 45:10191–10198

    Article  CAS  PubMed  Google Scholar 

  60. Purcell EB, Siegal-Gaskins D, Rawling DC et al (2007) A photosensory two-component system regulates bacterial cell attachment. Proc Natl Acad Sci USA 104:18241–18246

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  61. Swartz TE, Tseng T-S, Frederickson MA et al (2007) Blue-light-activated histidine kinases: two-component sensors in bacteria. Science 317:1090–1093

    Article  CAS  PubMed  Google Scholar 

  62. Christie JM, Salomon M, Nozue K et al (1999) LOV (light, oxygen, or voltage) domains of the blue-light photoreceptor phototropin (nph1): binding sites for the chromophore flavin mononucleotide. Proc Natl Acad Sci USA 96:8779–8783

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Liu C, Liew CW, Wong YH 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. https://doi.org/10.1128/JB.00515-17

    Article  PubMed  PubMed Central  Google Scholar 

  64. Kelley LA, Mezulis S, Yates CM et al (2015) The Phyre2 web portal for protein modeling, prediction and analysis. Nat Protoc 10:845–858

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  65. Yang J, Yan R, Roy A et al (2015) The I-TASSER Suite: protein structure and function prediction. Nat Methods 12:7–8

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. Brunger AT (2013) CNS (Crystallography and NMR System). In: Roberts GCK (ed) Encyclopedia of biophysics. Springer, Berlin, pp 326–327

    Chapter  Google Scholar 

  67. Adams PD, Afonine PV, Bunkóczi G et al (2010) PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr D Biol Crystallogr 66:213–221

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  68. McRee DE (1999) XtalView/Xfit – a versatile program for manipulating atomic coordinates and electron density. J Struct Biol 125:156–165

    Article  CAS  PubMed  Google Scholar 

  69. Schrodinger LLC (2015) The PyMOL molecular graphics system Version 1.8.0

    Google Scholar 

  70. Key J, Hefti M, Purcell EB, Moffat K (2007) Structure of the redox sensor domain of Azotobacter vinelandii NifL at atomic resolution: signaling, dimerization, and mechanism. Biochemistry 46:3614–3623

    Article  CAS  PubMed  Google Scholar 

  71. Park H, Suquet C, Satterlee JD, Kang C (2004) Insights into signal transduction involving PAS domain oxygen-sensing heme proteins from the X-ray crystal structure of Escherichia coli Dos heme domain (Ec DosH). Biochemistry 43:2738–2746

    Article  CAS  PubMed  Google Scholar 

  72. Airola MV, Huh D, Sukomon N et al (2013) Architecture of the soluble receptor Aer2 indicates an in-line mechanism for PAS and HAMP domain signaling. J Mol Biol 425:886–901

    Article  CAS  PubMed  Google Scholar 

  73. Miyatake H, Mukai M, Park SY et al (2000) Sensory mechanism of oxygen sensor FixL from Rhizobium meliloti: crystallographic, mutagenesis and resonance Raman spectroscopic studies. J Mol Biol 301:415–431

    Article  CAS  PubMed  Google Scholar 

  74. Hengge R, Galperin MY, Ghigo J-M et al (2016) Systematic nomenclature for GGDEF and EAL domain-containing cyclic di-GMP turnover proteins of Escherichia coli. J Bacteriol 198:7–11

    Article  CAS  PubMed  Google Scholar 

  75. Pesavento C, Becker G, Sommerfeldt N et al (2008) Inverse regulatory coordination of motility and curli-mediated adhesion in Escherichia coli. Genes Dev 22:2434–2446

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  76. Lindenberg S, Klauck G, Pesavento C et al (2013) The EAL domain protein YciR acts as a trigger enzyme in a c-di-GMP signalling cascade in E. coli biofilm control. EMBO J 32:2001–2014

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  77. Kulasakara H, Lee V, Brencic A 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 

  78. Ha D-G, Richman ME, O’Toole GA (2014) Deletion mutant library for investigation of functional outputs of cyclic diguanylate metabolism in Pseudomonas aeruginosa PA14. Appl Environ Microbiol 80:3384–3393

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  79. Christen M, Kulasekara HD, Christen B et al (2010) Asymmetrical distribution of the second messenger c-di-GMP upon bacterial cell division. Science 328:1295–1297

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  80. Moura-Alves P, Faé K, Houthuys E et al (2014) AhR sensing of bacterial pigments regulates antibacterial defence. Nature 512:387–392

    Article  CAS  PubMed  Google Scholar 

  81. Xu N, Ahuja EG, Janning P et al (2013) Trapped intermediates in crystals of the FMN-dependent oxidase PhzG provide insight into the final steps of phenazine biosynthesis. Acta Crystallogr D Biol Crystallogr 69:1403–1413

    Article  CAS  PubMed  Google Scholar 

  82. Schulte KW, Green E, Wilz A et al (2017) Structural basis for aryl hydrocarbon receptor-mediated gene activation. Structure 25:1025–1033.e3

    Article  CAS  PubMed  Google Scholar 

  83. An S, Wu J, Zhang L-H (2010) Modulation of Pseudomonas aeruginosa biofilm dispersal by a cyclic-di-GMP phosphodiesterase with a putative hypoxia-sensing domain. Appl Environ Microbiol 76:8160–8173

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  84. Paiardini A, Mantoni F, Giardina G et al (2018) A novel bacterial l-arginine sensor controlling c-di-GMP levels in Pseudomonas aeruginosa. Proteins Struct Funct Bioinf 86:1088–1096

    Article  CAS  Google Scholar 

  85. Sakhtah H, Koyama L, Zhang Y et al (2016) The Pseudomonas aeruginosa efflux pump MexGHI-OpmD transports a natural phenazine that controls gene expression and biofilm development. Proc Natl Acad Sci USA 113:E3538–E3547

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  86. Zhou L, Zhang L-H, Cámara M, He Y-W (2017) The DSF family of quorum sensing signals: diversity, biosynthesis, and turnover. Trends Microbiol 25:293–303

    Article  CAS  PubMed  Google Scholar 

  87. Mantoni F, Paiardini A, Brunotti P 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 

  88. Römling U, Galperin MY (2015) Bacterial cellulose biosynthesis: diversity of operons, subunits, products, and functions. Trends Microbiol 23:545–557

    Article  PubMed  PubMed Central  CAS  Google Scholar 

Download references

Acknowledgments

Research in the Dietrich laboratory is supported by NIH/NIAID grant R01AI103369 and an NSF CAREER award. Dr. Forouhar’s research is supported by NCI grant UR007972. Dr. Harrison’s research is supported by a Canada Research Chair and a Project Scheme Grant from the Canadian Institutes for Health Research (CIHR).

Author information

Author notes

  1. Authors Hannah Dayton and Marina K. Smiley contributed equally to this chapter.

Authors and Affiliations

  1. Department of Biological Sciences, Columbia University, New York, NY, USA

    Hannah Dayton, Marina K. Smiley, Alexa Price-Whelan & Lars E. P. Dietrich

  2. Irving Cancer Research Center, Columbia University Medical Center, New York, NY, USA

    Farhad Forouhar

  3. Department of Biological Sciences, University of Calgary, Calgary, AB, Canada

    Joe J. Harrison

Authors
  1. Hannah Dayton
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Marina K. Smiley
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Farhad Forouhar
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Joe J. Harrison
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Alexa Price-Whelan
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Lars E. P. Dietrich
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Lars E. P. Dietrich .

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

Dayton, H., Smiley, M.K., Forouhar, F., Harrison, J.J., Price-Whelan, A., Dietrich, L.E.P. (2020). Sensory Domains That Control Cyclic di-GMP-Modulating Proteins: A Critical Frontier in Bacterial Signal Transduction. 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_9

Download citation

Publish with us

Policies and ethics

Search

Navigation