Advertisement

Cyclic di-GMP Regulation of Gene Expression

  • Meng-Lun Hsieh
  • Deborah M. HintonEmail author
  • Christopher M. WatersEmail author
Chapter
  • 118 Downloads

Abstract

Cyclic di-GMP is a nearly ubiquitous bacterial second messenger signaling molecule that links changes in environmental cues to the regulation of a myriad of phenotypes including but not limited to biofilm formation, motility, virulence, and DNA repair. A complex network of cyclic di-GMP synthesis and degradation enzymes is present in many bacteria, each of which is hypothesized to respond to a different signal that is integrated into changes in cyclic di-GMP levels. Cyclic di-GMP regulates downstream phenotypes via a variety of different mechanisms including control of transcription initiation via direct interaction with transcription factors, binding to RNA riboswitches to control gene expression post-transcriptionally, or direct interaction with enzymes or protein complexes to allosterically regulate their activity. In this chapter, we will review what is known about cyclic di-GMP regulation of gene expression, both transcriptionally and post-transcriptionally, focusing on transcription factors and riboswitches that directly bind to cyclic di-GMP.

Keywords

Cyclic di-GMP Transcription Transcription factor Riboswitch 

References

  1. 1.
    Ausmees N, Mayer R, Weinhouse H, Volman G, Amikam D, Benziman M, Lindberg M (2001) Genetic data indicate that proteins containing the GGDEF domain possess diguanylate cyclase activity. FEMS Microbiol Lett 204(1):163–167CrossRefGoogle Scholar
  2. 2.
    Barends TR, Hartmann E, Griese JJ, Beitlich T, Kirienko NV, Ryjenkov DA, Reinstein J, Shoeman RL, Gomelsky M, Schlichting I (2009) Structure and mechanism of a bacterial light-regulated cyclic nucleotide phosphodiesterase. Nature 459(7249):1015–1018.  https://doi.org/10.1038/nature07966 CrossRefPubMedPubMedCentralGoogle Scholar
  3. 3.
    Chan C, Paul R, Samoray D, Amiot NC, Giese B, Jenal U, Schirmer T (2004) Structural basis of activity and allosteric control of diguanylate cyclase. Proc Natl Acad Sci USA 101(49):17084–17089CrossRefGoogle Scholar
  4. 4.
    Cohen D, Mechold U, Nevenzal H, Yarmiyhu Y, Randall TE, Bay DC, Rich JD, Parsek MR, Kaever V, Harrison JJ, Banin E (2015) Oligoribonuclease is a central feature of cyclic diguanylate signaling in Pseudomonas aeruginosa. Proc Natl Acad Sci USA 112(36):11359–11364.  https://doi.org/10.1073/pnas.1421450112 CrossRefPubMedPubMedCentralGoogle Scholar
  5. 5.
    Orr MW, Donaldson GP, Severin GB, Wang J, Sintim HO, Waters CM, Lee VT (2015) Oligoribonuclease is the primary degradative enzyme for pGpG in Pseudomonas aeruginosa that is required for cyclic-di-GMP turnover. Proc Natl Acad Sci USA 112(36):E5048–E5057.  https://doi.org/10.1073/pnas.1507245112 CrossRefPubMedPubMedCentralGoogle Scholar
  6. 6.
    Galperin MY (2004) Bacterial signal transduction network in a genomic perspective. Environ Microbiol 6(6):552–567CrossRefGoogle Scholar
  7. 7.
    Galperin MY, Nikolskaya AN, Koonin EV (2001) Novel domains of the prokaryotic two-component signal transduction systems. FEMS Microbiol Lett 203(1):11–21CrossRefGoogle Scholar
  8. 8.
    McKee RW, Kariisa A, Mudrak B, Whitaker C, Tamayo R (2014) A systematic analysis of the in vitro and in vivo functions of the HD-GYP domain proteins of Vibrio cholerae. BMC Microbiol 14:272.  https://doi.org/10.1186/s12866-014-0272-9 CrossRefPubMedPubMedCentralGoogle Scholar
  9. 9.
    Chang AL, Tuckerman JR, Gonzalez G, Mayer R, Weinhouse H, Volman G, Amikam D, Benziman M, Gilles-Gonzalez MA (2001) Phosphodiesterase A1, a regulator of cellulose synthesis in Acetobacter xylinum, is a heme-based sensor. Biochemistry 40(12):3420–3426CrossRefGoogle Scholar
  10. 10.
    Sasakura Y, Hirata S, Sugiyama S, Suzuki S, Taguchi S, Watanabe M, Matsui T, Sagami I, Shimizu T (2002) Characterization of a direct oxygen sensor heme protein from Escherichia coli. Effects of the heme redox states and mutations at the heme-binding site on catalysis and structure. J Biol Chem 277(26):23821–23827.  https://doi.org/10.1074/jbc.M202738200 CrossRefPubMedGoogle Scholar
  11. 11.
    Jenal U, Malone J (2006) Mechanisms of cyclic-di-GMP signaling in bacteria. Annu Rev Genet 40:385–407CrossRefGoogle Scholar
  12. 12.
    Hengge R (2009) Principles of c-di-GMP signalling in bacteria. Nat Rev Microbiol 7(4):263–273.  https://doi.org/10.1038/nrmicro2109 CrossRefGoogle Scholar
  13. 13.
    Pursley BR, Maiden MM, Hsieh ML, Fernandez NL, Severin GB, Waters CM (2018) Cyclic di-GMP regulates TfoY in Vibrio cholerae to control motility by both transcriptional and posttranscriptional mechanisms. J Bacteriol 200(7):578–617.  https://doi.org/10.1128/JB.00578-17 CrossRefGoogle Scholar
  14. 14.
    Fernandez NL, Srivastava D, Ngouajio AL, Waters CM (2018) Cyclic di-GMP positively regulates DNA repair in Vibrio cholerae. J Bacteriol 200(15).  https://doi.org/10.1128/JB.00005-18
  15. 15.
    Decker KB, Hinton DM (2013) Transcription regulation at the core: similarities among bacterial, archaeal, and eukaryotic RNA polymerases. Annu Rev Microbiol 67:113–139.  https://doi.org/10.1146/annurev-micro-092412-155756 CrossRefPubMedGoogle Scholar
  16. 16.
    Lee DJ, Minchin SD, Busby SJ (2012) Activating transcription in bacteria. Annu Rev Microbiol 66:125–152.  https://doi.org/10.1146/annurev-micro-092611-150012 CrossRefPubMedGoogle Scholar
  17. 17.
    Paget MS, Helmann JD (2003) The sigma70 family of sigma factors. Genome Biol 4(1):203CrossRefGoogle Scholar
  18. 18.
    Feklistov A, Sharon BD, Darst SA, Gross CA (2014) Bacterial sigma factors: a historical, structural, and genomic perspective. Annu Rev Microbiol 68:357–376.  https://doi.org/10.1146/annurev-micro-092412-155737 CrossRefPubMedGoogle Scholar
  19. 19.
    Bush M, Dixon R (2012) The role of bacterial enhancer binding proteins as specialized activators of sigma54-dependent transcription. Microbiol Mol Biol Rev 76(3):497–529.  https://doi.org/10.1128/MMBR.00006-12 CrossRefPubMedPubMedCentralGoogle Scholar
  20. 20.
    Zhang N, Buck M (2015) A perspective on the enhancer dependent bacterial RNA polymerase. Biomol Ther 5(2):1012–1019.  https://doi.org/10.3390/biom5021012 CrossRefGoogle Scholar
  21. 21.
    Zhang N, Darbari VC, Glyde R, Zhang X, Buck M (2016) The bacterial enhancer-dependent RNA polymerase. Biochem J 473(21):3741–3753.  https://doi.org/10.1042/BCJ20160741C CrossRefPubMedPubMedCentralGoogle Scholar
  22. 22.
    Srivastava D, Hsieh ML, Khataokar A, Neiditch MB, Waters CM (2013) Cyclic di-GMP inhibits Vibrio cholerae motility by repressing induction of transcription and inducing extracellular polysaccharide production. Mol Microbiol 90(6):1262–1276.  https://doi.org/10.1111/mmi.12432 CrossRefPubMedGoogle Scholar
  23. 23.
    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(5):1574–1578CrossRefGoogle Scholar
  24. 24.
    Yildiz FH, Dolganov NA, Schoolnik GK (2001) VpsR, a member of the response regulators of the two-component regulatory systems, is required for expression of vps biosynthesis genes and EPS(ETr)-associated phenotypes in Vibrio cholerae O1 El Tor. J Bacteriol 183(5):1716–1726.  https://doi.org/10.1128/JB.183.5.1716-1726.2001 CrossRefPubMedPubMedCentralGoogle Scholar
  25. 25.
    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(2):388–402.  https://doi.org/10.1128/JB.00981-06 CrossRefPubMedGoogle Scholar
  26. 26.
    Yildiz FH, Liu XS, Heydorn A, Schoolnik GK (2004) Molecular analysis of rugosity in a Vibrio cholerae O1 El Tor phase variant. Mol Microbiol 53(2):497–515.  https://doi.org/10.1111/j.1365-2958.2004.04154.x CrossRefPubMedGoogle Scholar
  27. 27.
    Krasteva PV, Fong JC, Shikuma NJ, Beyhan S, Navarro MV, Yildiz FH, Sondermann H (2010) Vibrio cholerae VpsT regulates matrix production and motility by directly sensing cyclic di-GMP. Science 327(5967):866–868.  https://doi.org/10.1126/science.1181185 CrossRefPubMedPubMedCentralGoogle Scholar
  28. 28.
    Zamorano-Sanchez D, Fong JC, Kilic S, Erill I, Yildiz FH (2015) Identification and characterization of VpsR and VpsT binding sites in Vibrio cholerae. J Bacteriol 197(7):1221–1235.  https://doi.org/10.1128/JB.02439-14 CrossRefPubMedPubMedCentralGoogle Scholar
  29. 29.
    Wang H, Ayala JC, Silva AJ, Benitez JA (2012) The histone-like nucleoid structuring protein (H-NS) is a repressor of Vibrio cholerae exopolysaccharide biosynthesis (vps) genes. Appl Environ Microbiol 78(7):2482–2488.  https://doi.org/10.1128/AEM.07629-11 CrossRefPubMedPubMedCentralGoogle Scholar
  30. 30.
    Wang H, Ayala JC, Benitez JA, Silva AJ (2014) The LuxR-type regulator VpsT negatively controls the transcription of rpoS, encoding the general stress response regulator, in Vibrio cholerae biofilms. J Bacteriol 196(5):1020–1030.  https://doi.org/10.1128/JB.00993-13 CrossRefPubMedPubMedCentralGoogle Scholar
  31. 31.
    Hsieh ML, Hinton DM, Waters CM (2018) VpsR and cyclic di-GMP together drive transcription initiation to activate biofilm formation in Vibrio cholerae. Nucleic Acids Res 46(17):8876–8887.  https://doi.org/10.1093/nar/gky606 CrossRefPubMedPubMedCentralGoogle Scholar
  32. 32.
    Matsuyama BY, Krasteva PV, Baraquet C, Harwood CS, Sondermann H, Navarro MV (2016) Mechanistic insights into c-di-GMP-dependent control of the biofilm regulator FleQ from Pseudomonas aeruginosa. Proc Natl Acad Sci USA 113(2):E209–E218.  https://doi.org/10.1073/pnas.1523148113 CrossRefGoogle Scholar
  33. 33.
    Srivastava D, Harris RC, Waters CM (2011) Integration of cyclic di-GMP and quorum sensing in the control of vpsT and aphA in Vibrio cholerae. J Bacteriol 193(22):6331–6341.  https://doi.org/10.1128/JB.05167-11 CrossRefPubMedPubMedCentralGoogle Scholar
  34. 34.
    Baraquet C, Harwood CS (2015) FleQ DNA binding consensus sequence revealed by studies of FleQ-dependent regulation of biofilm gene expression in Pseudomonas aeruginosa. J Bacteriol 198(1):178–186.  https://doi.org/10.1128/JB.00539-15 CrossRefPubMedPubMedCentralGoogle Scholar
  35. 35.
    Baraquet C, Harwood CS (2013) Cyclic diguanosine monophosphate represses bacterial flagella synthesis by interacting with the Walker A motif of the enhancer-binding protein FleQ. Proc Natl Acad Sci USA 110(46):18478–18483.  https://doi.org/10.1073/pnas.1318972110 CrossRefPubMedPubMedCentralGoogle Scholar
  36. 36.
    Baraquet C, Murakami K, Parsek MR, Harwood CS (2012) 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 40(15):7207–7218.  https://doi.org/10.1093/nar/gks384 CrossRefPubMedPubMedCentralGoogle Scholar
  37. 37.
    Jyot J, Dasgupta N, Ramphal R (2002) FleQ, the major flagellar gene regulator in Pseudomonas aeruginosa, binds to enhancer sites located either upstream or atypically downstream of the RpoN binding site. J Bacteriol 184(19):5251–5260CrossRefGoogle Scholar
  38. 38.
    Arora SK, Ritchings BW, Almira EC, Lory S, Ramphal R (1997) A transcriptional activator, FleQ, regulates mucin adhesion and flagellar gene expression in Pseudomonas aeruginosa in a cascade manner. J Bacteriol 179(17):5574–5581CrossRefGoogle Scholar
  39. 39.
    Wang F, He Q, Yin J, Xu S, Hu W, Gu L (2018) BrlR from Pseudomonas aeruginosa is a receptor for both cyclic di-GMP and pyocyanin. Nat Commun 9(1):2563.  https://doi.org/10.1038/s41467-018-05004-y CrossRefPubMedPubMedCentralGoogle Scholar
  40. 40.
    Liao J, Schurr MJ, Sauer K (2013) The MerR-like regulator BrlR confers biofilm tolerance by activating multidrug efflux pumps in Pseudomonas aeruginosa biofilms. J Bacteriol 195(15):3352–3363.  https://doi.org/10.1128/JB.00318-13 CrossRefPubMedPubMedCentralGoogle Scholar
  41. 41.
    Chambers JR, Liao J, Schurr MJ, Sauer K (2014) BrlR from Pseudomonas aeruginosa is a c-di-GMP-responsive transcription factor. Mol Microbiol 92(3):471–487.  https://doi.org/10.1111/mmi.12562 CrossRefPubMedPubMedCentralGoogle Scholar
  42. 42.
    Raju H, Sharma R (2017) Crystal structure of BrlR with c-di-GMP. Biochem Biophys Res Commun 490(2):260–264.  https://doi.org/10.1016/j.bbrc.2017.06.033 CrossRefPubMedGoogle Scholar
  43. 43.
    Wilksch JJ, Yang J, Clements A, Gabbe JL, Short KR, Cao H, Cavaliere R, James CE, Whitchurch CB, Schembri MA, Chuah ML, Liang ZX, Wijburg OL, Jenney AW, Lithgow T, Strugnell RA (2011) MrkH, a novel c-di-GMP-dependent transcriptional activator, controls Klebsiella pneumoniae biofilm formation by regulating type 3 fimbriae expression. PLoS Pathog 7(8):e1002204.  https://doi.org/10.1371/journal.ppat.1002204 CrossRefPubMedPubMedCentralGoogle Scholar
  44. 44.
    Tan JW, Wilksch JJ, Hocking DM, Wang N, Srikhanta YN, Tauschek M, Lithgow T, Robins-Browne RM, Yang J, Strugnell RA (2015) Positive autoregulation of mrkHI by the cyclic di-GMP-dependent MrkH protein in the biofilm regulatory circuit of Klebsiella pneumoniae. J Bacteriol 197(9):1659–1667.  https://doi.org/10.1128/JB.02615-14 CrossRefPubMedPubMedCentralGoogle Scholar
  45. 45.
    Yang J, Wilksch JJ, Tan JW, Hocking DM, Webb CT, Lithgow T, Robins-Browne RM, Strugnell RA (2013) Transcriptional activation of the mrkA promoter of the Klebsiella pneumoniae type 3 fimbrial operon by the c-di-GMP-dependent MrkH protein. PLoS One 8(11):e79038.  https://doi.org/10.1371/journal.pone.0079038 CrossRefPubMedPubMedCentralGoogle Scholar
  46. 46.
    Schumacher MA, Zeng W (2016) Structures of the activator of K. pneumonia biofilm formation, MrkH, indicates PilZ domains involved in c-di-GMP and DNA binding. Proc Natl Acad Sci USA 113(36):10067–10072.  https://doi.org/10.1073/pnas.1607503113 CrossRefPubMedGoogle Scholar
  47. 47.
    Fazli M, McCarthy Y, Givskov M, Ryan RP, Tolker-Nielsen T (2013) The exopolysaccharide gene cluster Bcam1330-Bcam1341 is involved in Burkholderia cenocepacia biofilm formation, and its expression is regulated by c-di-GMP and Bcam1349. Microbiol Open 2(1):105–122.  https://doi.org/10.1002/mbo3.61 CrossRefGoogle Scholar
  48. 48.
    Fazli M, O’Connell A, Nilsson M, Niehaus K, Dow JM, Givskov M, Ryan RP, Tolker-Nielsen T (2011) The CRP/FNR family protein Bcam1349 is a c-di-GMP effector that regulates biofilm formation in the respiratory pathogen Burkholderia cenocepacia. Mol Microbiol 82(2):327–341.  https://doi.org/10.1111/j.1365-2958.2011.07814.x CrossRefGoogle Scholar
  49. 49.
    Fazli M, Rybtke M, Steiner E, Weidel E, Berthelsen J, Groizeleau J, Bin W, Zhi BZ, Yaming Z, Kaever V, Givskov M, Hartmann RW, Eberl L, Tolker-Nielsen T (2017) Regulation of Burkholderia cenocepacia biofilm formation by RpoN and the c-di-GMP effector BerB. Microbiol Open 6(4).  https://doi.org/10.1002/mbo3.480 CrossRefGoogle Scholar
  50. 50.
    Chin KH, Lee YC, Tu ZL, Chen CH, Tseng YH, Yang JM, Ryan RP, McCarthy Y, Dow JM, Wang AH, Chou SH (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 Bio 396(3):646–662.  https://doi.org/10.1016/j.jmb.2009.11.076 CrossRefGoogle Scholar
  51. 51.
    den Hengst CD, Tran NT, Bibb MJ, Chandra G, Leskiw BK, Buttner MJ (2010) Genes essential for morphological development and antibiotic production in Streptomyces coelicolor are targets of BldD during vegetative growth. Mol Microbiol 78(2):361–379CrossRefGoogle Scholar
  52. 52.
    Elliot MA, Bibb MJ, Buttner MJ, Leskiw BK (2001) BldD is a direct regulator of key developmental genes in Streptomyces coelicolor A3(2). Mol Microbiol 40(1):257–269CrossRefGoogle Scholar
  53. 53.
    Tschowri N, Schumacher MA, Schlimpert S, Chinnam NB, Findlay KC, Brennan RG, Buttner MJ (2014) Tetrameric c-di-GMP mediates effective transcription factor dimerization to control Streptomyces development. Cell 158(5):1136–1147.  https://doi.org/10.1016/j.cell.2014.07.022 CrossRefPubMedPubMedCentralGoogle Scholar
  54. 54.
    Schumacher MA, Zeng W, Findlay KC, Buttner MJ, Brennan RG, Tschowri N (2017) The Streptomyces master regulator BldD binds c-di-GMP sequentially to create a functional BldD2-(c-di-GMP)4 complex. Nucleic Acids Res 45(11):6923–6933.  https://doi.org/10.1093/nar/gkx287 CrossRefPubMedPubMedCentralGoogle Scholar
  55. 55.
    Li W, He ZG (2012) LtmA, a novel cyclic di-GMP-responsive activator, broadly regulates the expression of lipid transport and metabolism genes in Mycobacterium smegmatis. Nucleic Acids Res 40(22):11292–11307.  https://doi.org/10.1093/nar/gks923 CrossRefPubMedPubMedCentralGoogle Scholar
  56. 56.
    Li W, Li M, Hu L, Zhu J, Xie Z, Chen J, He ZG (2018) HpoR, a novel c-di-GMP effective transcription factor, links the second messenger’s regulatory function to the mycobacterial antioxidant defense. Nucleic Acids Res 46(7):3595–3611.  https://doi.org/10.1093/nar/gky146 CrossRefPubMedPubMedCentralGoogle Scholar
  57. 57.
    Li W, Hu L, Xie Z, Xu H, Li M, Cui T, He ZG (2018) Cyclic di-GMP integrates functionally divergent transcription factors into a regulation pathway for antioxidant defense. Nucleic Acids Res 46(14):7270–7283.  https://doi.org/10.1093/nar/gky611 CrossRefPubMedPubMedCentralGoogle Scholar
  58. 58.
    Shanahan CA, Strobel SA (2012) The bacterial second messenger c-di-GMP: probing interactions with protein and RNA binding partners using cyclic dinucleotide analogs. Org Biomol Chem 10(46):9113–9129.  https://doi.org/10.1039/c2ob26724a CrossRefPubMedPubMedCentralGoogle Scholar
  59. 59.
    Baird NJ, Kulshina N, Ferre-D’Amare AR (2010) Riboswitch function: flipping the switch or tuning the dimmer? RNA Biol 7(3):328–332CrossRefGoogle Scholar
  60. 60.
    Martinez LC, Vadyvaloo V (2014) Mechanisms of post-transcriptional gene regulation in bacterial biofilms. Front Cell Infect Microbiol 4:38.  https://doi.org/10.3389/fcimb.2014.00038 CrossRefPubMedPubMedCentralGoogle Scholar
  61. 61.
    Lee ER, Baker JL, Weinberg Z, Sudarsan N, Breaker RR (2010) An allosteric self-splicing ribozyme triggered by a bacterial second messenger. Science 329(5993):845–848.  https://doi.org/10.1126/science.1190713 CrossRefPubMedPubMedCentralGoogle Scholar
  62. 62.
    Chen AG, Sudarsan N, Breaker RR (2011) Mechanism for gene control by a natural allosteric group I ribozyme. RNA 17(11):1967–1972.  https://doi.org/10.1261/rna.2757311 CrossRefPubMedPubMedCentralGoogle Scholar
  63. 63.
    Sudarsan N, Lee ER, Weinberg Z, Moy RH, Kim JN, Link KH, Breaker RR (2008) Riboswitches in eubacteria sense the second messenger cyclic di-GMP. Science 321(5887):411–413.  https://doi.org/10.1126/science.1159519 CrossRefPubMedPubMedCentralGoogle Scholar
  64. 64.
    Purcell EB, McKee RW, McBride SM, Waters CM, Tamayo R (2012) Cyclic diguanylate inversely regulates motility and aggregation in Clostridium difficile. J Bacteriol 194(13):3307–3316.  https://doi.org/10.1128/JB.00100-12 CrossRefPubMedPubMedCentralGoogle Scholar
  65. 65.
    McKee RW, Aleksanyan N, Garrett EM, Tamayo R (2018) Type IV pili promote Clostridium difficile adherence and persistence in a mouse model of infection. Infect Immun 86(5).  https://doi.org/10.1128/IAI.00943-17
  66. 66.
    Bordeleau E, Purcell EB, Lafontaine DA, Fortier LC, Tamayo R, Burrus V (2015) Cyclic di-GMP riboswitch-regulated type IV pili contribute to aggregation of Clostridium difficile. J Bacteriol 197(5):819–832.  https://doi.org/10.1128/JB.02340-14 CrossRefPubMedPubMedCentralGoogle Scholar
  67. 67.
    McKee RW, Harvest CK, Tamayo R (2018) Cyclic diguanylate regulates virulence factor genes via multiple riboswitches in Clostridium difficile. mSphere 3(5).  https://doi.org/10.1128/mSphere.00423-18
  68. 68.
    Metzger LC, Stutzmann S, Scrignari T, Van der Henst C, Matthey N, Blokesch M (2016) Independent regulation of type VI secretion in Vibrio cholerae by TfoX and TfoY. Cell Rep 15(5):951–958.  https://doi.org/10.1016/j.celrep.2016.03.092 CrossRefPubMedPubMedCentralGoogle Scholar
  69. 69.
    Inuzuka S, Kakizawa H, Nishimura KI, Naito T, Miyazaki K, Furuta H, Matsumura S, Ikawa Y (2018) Recognition of cyclic-di-GMP by a riboswitch conducts translational repression through masking the ribosome-binding site distant from the aptamer domain. Genes Cells 23(6):435–447.  https://doi.org/10.1111/gtc.12586 CrossRefPubMedGoogle Scholar
  70. 70.
    Inuzuka S, Nishimura K, Kakizawa H, Fujita Y, Furuta H, Matsumura S, Ikawa Y (2016) Mutational analysis of structural elements in a class-I cyclic di-GMP riboswitch to elucidate its regulatory mechanism. J Biochem 160(3):153–162.  https://doi.org/10.1093/jb/mvw026 CrossRefPubMedGoogle Scholar
  71. 71.
    Kariisa AT, Weeks K, Tamayo R (2016) The RNA domain Vc1 regulates downstream gene expression in response to cyclic diguanylate in Vibrio cholerae. PLoS One 11(2):e0148478.  https://doi.org/10.1371/journal.pone.0148478 CrossRefPubMedPubMedCentralGoogle Scholar
  72. 72.
    Karunker I, Rotem O, Dori-Bachash M, Jurkevitch E, Sorek R (2013) A global transcriptional switch between the attack and growth forms of Bdellovibrio bacteriovorus. PLoS One 8(4):e61850.  https://doi.org/10.1371/journal.pone.0061850 CrossRefPubMedPubMedCentralGoogle Scholar
  73. 73.
    Tang Q, Yin K, Qian H, Zhao Y, Wang W, Chou SH, Fu Y, He J (2016) Cyclic di-GMP contributes to adaption and virulence of Bacillus thuringiensis through a riboswitch-regulated collagen adhesion protein. Sci Rep 6:28807.  https://doi.org/10.1038/srep28807 CrossRefPubMedPubMedCentralGoogle Scholar
  74. 74.
    Dippel AB, Anderson WA, Evans RS, Deutsch S, Hammond MC (2018) Chemiluminescent biosensors for detection of second messenger cyclic di-GMP. ACS Chem Biol 13(7):1872–1879.  https://doi.org/10.1021/acschembio.7b01019 CrossRefPubMedPubMedCentralGoogle Scholar
  75. 75.
    Hickman JW, Harwood CS (2008) Identification of FleQ from Pseudomonas aeruginosa as a c-di-GMP-responsive transcription factor. Mol Microbiol 69(2):376–389.  https://doi.org/10.1111/j.1365-2958.2008.06281.x CrossRefPubMedPubMedCentralGoogle Scholar
  76. 76.
    Lindenberg S, Klauck G, Pesavento C, Klauck E, Hengge R (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(14):2001–2014.  https://doi.org/10.1038/emboj.2013.120 CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2020

Authors and Affiliations

  1. 1.Department of Biochemistry and Molecular BiologyMichigan State UniversityEast LansingUSA
  2. 2.Gene Expression and Regulation Section, Laboratory of Cell and Molecular BiologyNational Institute of Diabetes and Digestive and Kidney Diseases, National Institutes of HealthBethesdaUSA
  3. 3.Department of Microbiology and Molecular GeneticsMichigan State UniversityEast LansingUSA

Personalised recommendations