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Cyclic di-GMP Signaling in Salmonella enterica serovar Typhimurium

  • Ute RömlingEmail author
Chapter
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Abstract

Cyclic di-GMP is perhaps the most abundant nucleotide-based second messenger in bacteria. In the gamma-proteobacterium Salmonella enterica serovar Typhimurium, a gastrointestinal pathogen, this signaling network regulates biofilm formation, flagella-associated physiology, and acute virulence properties. This chapter summarizes the impact of the complex cyclic di-GMP signaling network on the physiology of S. typhimurium in different environments and compares its consequences, when appropriate, with the close relative, the commensal and pathogenic Escherichia coli. The substantial diversity and variability in the cyclic di-GMP turnover protein network span from single amino acid replacements and stop codon variants in individual proteins to deletion and acquisition of novel cyclic di-GMP turnover genes by horizontal transfer. Despite differences in enzyme activities and gene combinations, cyclic di-GMP signaling modules become integrated into a common but even isolate-specific regulation of lifestyle transitions that are coordinated with cell cycle regulation. On a wider phylogenetic perspective, the observed conservation of cyclic di-GMP turnover proteins with a similar domain structure found in S. enterica throughout the phylogenetic tree poses a quest for the origin and maintenance of common principles in cyclic di-GMP signaling.

Keywords

Cyclic di-GMP Diversity Salmonella typhimurium Escherichia coli Horizontal gene transfer 

Notes

Acknowledgments

UR appreciates the constructive comments of the reviewers of this manuscript and appreciates the engagement of former and present coworkers. Research in the laboratory of UR is supported by funding from the Swedish Research Council Natural Sciences and Engineering, Swedish Research Links, and the European Commission.

References

  1. 1.
    Ross P, Weinhouse H, Aloni Y, Michaeli D, Weinberger-Ohana P, Mayer R, Braun S, de Vroom E, van der Marel GA, van Boom JH, Benziman M (1987) Regulation of cellulose synthesis in Acetobacter xylinum by cyclic diguanylic acid. Nature 325(6101):279–281CrossRefGoogle Scholar
  2. 2.
    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(4):1123–1134.  https://doi.org/10.1111/j.1365-2958.2004.04206.x CrossRefPubMedPubMedCentralGoogle Scholar
  3. 3.
    Paul R, Weiser S, Amiot NC, Chan C, Schirmer T, Giese B, Jenal U (2004) Cell cycle-dependent dynamic localization of a bacterial response regulator with a novel di-guanylate cyclase output domain. Genes Dev 18(6):715–727.  https://doi.org/10.1101/gad.289504 CrossRefPubMedPubMedCentralGoogle Scholar
  4. 4.
    Tischler AD, Camilli A (2004) Cyclic diguanylate (c-di-GMP) regulates Vibrio cholerae biofilm formation. Mol Microbiol 53(3):857–869.  https://doi.org/10.1111/j.1365-2958.2004.04155.x CrossRefPubMedPubMedCentralGoogle Scholar
  5. 5.
    Wuichet K, Cantwell BJ, Zhulin IB (2010) Evolution and phyletic distribution of two-component signal transduction systems. Curr Opin Microbiol 13(2):219–225.  https://doi.org/10.1016/j.mib.2009.12.011 CrossRefPubMedPubMedCentralGoogle Scholar
  6. 6.
    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):1–52.  https://doi.org/10.1128/MMBR.00043-12 CrossRefPubMedPubMedCentralGoogle Scholar
  7. 7.
    Chou SH, Galperin MY (2016) Diversity of cyclic di-GMP-binding proteins and mechanisms. J Bacteriol 198(1):32–46.  https://doi.org/10.1128/JB.00333-15 CrossRefGoogle Scholar
  8. 8.
    Römling U, Sierralta WD, Eriksson K, Normark S (1998) Multicellular and aggregative behaviour of Salmonella typhimurium strains is controlled by mutations in the agfD promoter. Mol Microbiol 28(2):249–264CrossRefGoogle Scholar
  9. 9.
    Römling U, Rohde M, Olsen A, Normark S, Reinköster J (2000) AgfD, the checkpoint of multicellular and aggregative behaviour in Salmonella typhimurium regulates at least two independent pathways. Mol Microbiol 36(1):10–23CrossRefGoogle Scholar
  10. 10.
    Römling U, Bian Z, Hammar M, Sierralta WD, Normark S (1998) Curli fibers are highly conserved between Salmonella typhimurium and Escherichia coli with respect to operon structure and regulation. J Bacteriol 180(3):722–731CrossRefGoogle Scholar
  11. 11.
    Zakikhany K, Harrington CR, Nimtz M, Hinton JCD, Römling U (2010) Unphosphorylated CsgD controls biofilm formation in Salmonella enterica serovar Typhimurium. Mol Microbiol 77:771–786CrossRefGoogle Scholar
  12. 12.
    Zogaj X, Nimtz M, Rohde M, Bokranz W, Römling U (2001) The multicellular morphotypes of Salmonella typhimurium and Escherichia coli produce cellulose as the second component of the extracellular matrix. Mole Microbiol 39(6):1452–1463CrossRefGoogle Scholar
  13. 13.
    Römling U (2005) Characterization of the rdar morphotype, a multicellular behaviour in Enterobacteriaceae. Cell Mol Life Sci 62(11):1234–1246.  https://doi.org/10.1007/s00018-005-4557-x CrossRefPubMedGoogle Scholar
  14. 14.
    Rossi E, Motta S, Aliverti A, Cossu F, Gourlay L, Mauri P, Landini P (2017) Cellulose production is coupled to sensing of the pyrimidine biosynthetic pathway via c-di-GMP production by the DgcQ protein of Escherichia coli. Environ Microbiol 19(11):4551–4563.  https://doi.org/10.1111/1462-2920.13918 CrossRefPubMedGoogle Scholar
  15. 15.
    Andrade MO, Alegria MC, Guzzo CR, Docena C, Rosa MC, Ramos CH, Farah CS (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(2):537–551.  https://doi.org/10.1111/j.1365-2958.2006.05386.x CrossRefGoogle Scholar
  16. 16.
    Sarenko O, Klauck G, Wilke FM, Pfiffer V, Richter AM, Herbst S, Kaever V, Hengge R (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(5).  https://doi.org/10.1128/mBio.01639-17
  17. 17.
    Ahmad I, Lamprokostopoulou A, Le Guyon S, Streck E, Barthel M, Peters V, Hardt WD, Römling U (2011) Complex c-di-GMP signaling networks mediate transition between virulence properties and biofilm formation in Salmonella enterica serovar Typhimurium. PLoS One 6(12):e28351.  https://doi.org/10.1371/journal.pone.0028351 CrossRefPubMedPubMedCentralGoogle Scholar
  18. 18.
    Ahmad I, Wigren E, Le Guyon S, Vekkeli S, Blanka A, El Mouali Y, Anwar N, Chuah ML, Lünsdorf H, Frank R, Rhen M, Liang ZX, Lindqvist Y, Römling U (2013) The EAL-like protein STM1697 regulates virulence phenotypes, motility and biofilm formation in Salmonella typhimurium. Mol Microbiol 90(6):1216–1232.  https://doi.org/10.1111/mmi.12428 CrossRefGoogle Scholar
  19. 19.
    Wang KC, Hsu YH, Huang YN, Yeh KS (2012) A previously uncharacterized gene stm0551 plays a repressive role in the regulation of type 1 fimbriae in Salmonella enterica serotype Typhimurium. BMC Microbiol 12:111.  https://doi.org/10.1186/1471-2180-12-111 CrossRefPubMedPubMedCentralGoogle Scholar
  20. 20.
    Babitzke P, Lai YJ, Renda A, Romeo T (2019) Posttranscription initiation control of gene expression mediated by bacterial RNA-binding proteins. Annu Rev Microbiol 73:43–67.  https://doi.org/10.1146/annurev-micro-020518-115907 CrossRefGoogle Scholar
  21. 21.
    Galperin MY, Gaidenko TA, Mulkidjanian AY, Nakano M, Price CW (2001) MHYT, a new integral membrane sensor domain. FEMS Microbiol Lett 205(1):17–23.  https://doi.org/10.1111/j.1574-6968.2001.tb10919.x CrossRefGoogle Scholar
  22. 22.
    Ponting CP, Aravind L (1997) PAS: a multifunctional domain family comes to light. Curr Biol 7(11):R674–R677CrossRefGoogle Scholar
  23. 23.
    El Mouali Y, Kim H, Ahmad I, Brauner A, Liu Y, Skurnik M, Galperin MY, Römling U (2017) Stand-alone EAL domain proteins form a distinct subclass of EAL proteins involved in regulation of cell motility and biofilm formation in Enterobacteria. J Bacteriol 199(18):e00179-17.  https://doi.org/10.1128/JB.00179-17
  24. 24.
    Herbst S, Lorkowski M, Sarenko O, Nguyen TKL, Jaenicke T, Hengge R (2018) Transmembrane redox control and proteolysis of PdeC, a novel type of c-di-GMP phosphodiesterase. EMBO J 37(8):e97825.  https://doi.org/10.15252/embj.201797825
  25. 25.
    Römling U, Gomelsky M, Galperin MY (2005) C-di-GMP: the dawning of a novel bacterial signalling system. Mol Microbiol 57(3):629–639.  https://doi.org/10.1111/j.1365-2958.2005.04697.x CrossRefGoogle Scholar
  26. 26.
    Wada T, Morizane T, Abo T, Tominaga A, Inoue-Tanaka K, Kutsukake K (2011) EAL domain protein YdiV acts as an anti-FlhD4C2 factor responsible for nutritional control of the flagellar regulon in Salmonella enterica Serovar Typhimurium. J Bacteriol 193(7):1600–1611.  https://doi.org/10.1128/JB.01494-10 CrossRefPubMedPubMedCentralGoogle Scholar
  27. 27.
    Simm R, Remminghorst U, Ahmad I, Zakikhany K, Römling U (2009) A role for the EAL-like protein STM1344 in regulation of CsgD expression and motility in Salmonella enterica serovar Typhimurium. J Bacteriol 191(12):3928–3937.  https://doi.org/10.1128/JB.00290-09 CrossRefPubMedPubMedCentralGoogle Scholar
  28. 28.
    Nikolskaya AN, Mulkidjanian AY, Beech IB, Galperin MY (2003) MASE1 and MASE2: two novel integral membrane sensory domains. J Mol Microbiol Biotechnol 5(1):11–16.  https://doi.org/10.1159/000068720 CrossRefGoogle Scholar
  29. 29.
    Hengge R, Galperin MY, Ghigo JM, Gomelsky M, Green J, Hughes KT, Jenal U, Landini P (2015) Systematic nomenclature for GGDEF and EAL domain-containing c-di-GMP turnover proteins of Escherichia coli. J Bacteriol 198:7–11.  https://doi.org/10.1128/JB.00424-15 CrossRefPubMedPubMedCentralGoogle Scholar
  30. 30.
    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
  31. 31.
    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(10):2685–2691CrossRefGoogle Scholar
  32. 32.
    Mills E, Petersen E, Kulasekara BR, Miller SI (2015) A direct screen for c-di-GMP modulators reveals a Salmonella Typhimurium periplasmic L-arginine-sensing pathway. Sci Signal 8(380):ra57.  https://doi.org/10.1126/scisignal.aaa1796 CrossRefPubMedPubMedCentralGoogle Scholar
  33. 33.
    Römling U (2015) Small molecules with big effects: cyclic di-GMP-mediated stimulation of cellulose production by the amino acid L-arginine. Sci Signal 8(380):fs12.  https://doi.org/10.1126/scisignal.aac4734 CrossRefPubMedGoogle Scholar
  34. 34.
    Cowles KN, Willis DK, Engel TN, Jones JB, Barak JD (2016) Diguanylate cyclases AdrA and STM1987 regulate Salmonella enterica exopolysaccharide production during plant colonization in an environment-dependent manner. Appl Environ Microbiol 82(4):1237–1248.  https://doi.org/10.1128/AEM.03475-15 CrossRefPubMedPubMedCentralGoogle Scholar
  35. 35.
    Pfiffer V, Sarenko O, Possling A, Hengge R (2019) Genetic dissection of Escherichia coli’s master diguanylate cyclase DgcE: role of the N-terminal MASE1 domain and direct signal input from a GTPase partner system. PLoS Genet 15(4):e1008059.  https://doi.org/10.1371/journal.pgen.1008059 CrossRefPubMedPubMedCentralGoogle Scholar
  36. 36.
    Lacey M, Agasing A, Lowry R, Green J (2013) Identification of the YfgF MASE1 domain as a modulator of bacterial responses to aspartate. Open Biol 3(6):130046.  https://doi.org/10.1098/rsob.130046 CrossRefPubMedPubMedCentralGoogle Scholar
  37. 37.
    Yang C, Cui C, Ye Q, Kan J, Fu S, Song S, Huang Y, He F, Zhang LH, Jia Y, Gao YG, Harwood CS, Deng Y (2017) Burkholderia cenocepacia integrates cis-2-dodecenoic acid and cyclic dimeric guanosine monophosphate signals to control virulence. Proc Natl Acad Sci USA 114(49):13006–13011.  https://doi.org/10.1073/pnas.1709048114 CrossRefPubMedGoogle Scholar
  38. 38.
    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(16):3531–3542.  https://doi.org/10.1128/JB.01156-12 CrossRefPubMedPubMedCentralGoogle Scholar
  39. 39.
    Wang Y, Hay ID, Rehman ZU, Rehm BH (2015) Membrane-anchored MucR mediates nitrate-dependent regulation of alginate production in Pseudomonas aeruginosa. Appl Microbiol Biotechnol 99(17):7253–7265.  https://doi.org/10.1007/s00253-015-6591-4 CrossRefPubMedPubMedCentralGoogle Scholar
  40. 40.
    Fang X, Ahmad I, Blanka A, Schottkowski M, Cimdins A, Galperin MY, Römling U, Gomelsky M (2014) GIL, a new c-di-GMP-binding protein domain involved in regulation of cellulose synthesis in enterobacteria. Mol Microbiol 93(3):439–452.  https://doi.org/10.1111/mmi.12672 CrossRefPubMedPubMedCentralGoogle Scholar
  41. 41.
    Ryjenkov DA, Simm R, Römling 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(41):30310–30314.  https://doi.org/10.1074/jbc.C600179200 CrossRefGoogle Scholar
  42. 42.
    Trampari E, Stevenson CE, Little RH, Wilhelm T, Lawson DM, Malone JG (2015) Bacterial rotary export ATPases are allosterically regulated by the nucleotide second messenger cyclic-di-GMP. J Biol Chem 290(40):24470–24483.  https://doi.org/10.1074/jbc.M115.661439 CrossRefPubMedPubMedCentralGoogle Scholar
  43. 43.
    Amikam D, Galperin MY (2006) PilZ domain is part of the bacterial c-di-GMP binding protein. Bioinformatics 22(1):3–6.  https://doi.org/10.1093/bioinformatics/bti739 CrossRefGoogle Scholar
  44. 44.
    Cheang QW, Xin L, Chea RYF, Liang ZX (2019) Emerging paradigms for PilZ domain-mediated C-di-GMP signaling. Biochem Soc Trans 47(1):381–388.  https://doi.org/10.1042/BST20180543 CrossRefPubMedGoogle Scholar
  45. 45.
    Bai F, Morimoto YV, Yoshimura SD, Hara N, Kami-Ike N, Namba K, Minamino T (2014) Assembly dynamics and the roles of FliI ATPase of the bacterial flagellar export apparatus. Sci Rep 4:6528.  https://doi.org/10.1038/srep06528 CrossRefPubMedPubMedCentralGoogle Scholar
  46. 46.
    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
  47. 47.
    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 CrossRefPubMedPubMedCentralGoogle Scholar
  48. 48.
    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
  49. 49.
    Christen B, Christen M, Paul R, Schmid F, Folcher M, Jenoe P, Meuwly M, Jenal U (2006) Allosteric control of cyclic di-GMP signaling. J Biol Chem 281(42):32015–32024.  https://doi.org/10.1074/jbc.M603589200 CrossRefGoogle Scholar
  50. 50.
    Navarro MV, De N, Bae N, Wang Q, Sondermann H (2009) Structural analysis of the GGDEF-EAL domain-containing c-di-GMP receptor FimX. Structure 17(8):1104–1116.  https://doi.org/10.1016/j.str.2009.06.010 CrossRefPubMedPubMedCentralGoogle Scholar
  51. 51.
    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):17084–17089.  https://doi.org/10.1073/pnas.0406134101 CrossRefGoogle Scholar
  52. 52.
    Dahlström KM, Giglio KM, Sondermann H, O’Toole GA (2016) The inhibitory site of a diguanylate cyclase is a necessary element for interaction and signaling with an effector protein. J Bacteriol 198(11):1595–1603.  https://doi.org/10.1128/JB.00090-16 CrossRefPubMedPubMedCentralGoogle Scholar
  53. 53.
    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(6):1474–1484.  https://doi.org/10.1111/j.1365-2958.2007.05879.x CrossRefPubMedPubMedCentralGoogle Scholar
  54. 54.
    Duerig A, Abel S, Folcher M, Nicollier M, Schwede T, Amiot N, Giese B, Jenal U (2009) Second messenger-mediated spatiotemporal control of protein degradation regulates bacterial cell cycle progression. Genes Dev 23(1):93–104.  https://doi.org/10.1101/gad.502409 CrossRefPubMedPubMedCentralGoogle Scholar
  55. 55.
    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
  56. 56.
    Robert-Paganin J, Nonin-Lecomte S, Rety S (2012) Crystal structure of an EAL domain in complex with reaction product 5′-pGpG. PLoS One 7(12):e52424.  https://doi.org/10.1371/journal.pone.0052424 CrossRefPubMedPubMedCentralGoogle Scholar
  57. 57.
    Römling U, Liang ZX, Dow JM (2017) Progress in understanding the molecular basis underlying functional diversification of cyclic dinucleotide turnover proteins. J Bacteriol 199(5):e00790-16.  https://doi.org/10.1128/JB.00790-16
  58. 58.
    Duvel J, Bertinetti D, Moller S, Schwede F, Morr M, Wissing J, Radamm L, Zimmermann B, Genieser HG, Jänsch L, Herberg FW, Haussler S (2012) A chemical proteomics approach to identify c-di-GMP binding proteins in Pseudomonas aeruginosa. J Microbiol Methods 88(2):229–236.  https://doi.org/10.1016/j.mimet.2011.11.015 CrossRefGoogle Scholar
  59. 59.
    Nelson JW, Breaker RR (2017) The lost language of the RNA World. Sci Signal 10(483):e00790-16.  https://doi.org/10.1126/scisignal.aam8812 CrossRefGoogle Scholar
  60. 60.
    Kim HK, Harshey RM (2016) A diguanylate cyclase acts as a cell division inhibitor in a two-step response to reductive and envelope stresses. MBio 7(4):e00822-16.  https://doi.org/10.1128/mBio.00822-16
  61. 61.
    Poudyal B, Sauer K (2018) The PA3177 gene encodes an active diguanylate cyclase that contributes to biofilm antimicrobial tolerance but not biofilm formation by Pseudomonas aeruginosa. Antimicrob Agents Chemother 62(10):e01049-18.  https://doi.org/10.1128/AAC.01049-18
  62. 62.
    Simm R, Ahmad I, Rhen M, Le Guyon S, Römling U (2014) Regulation of biofilm formation in Salmonella enterica serovar Typhimurium. Future Microbiol 9(11):1261–1282.  https://doi.org/10.2217/fmb.14.88 CrossRefPubMedGoogle Scholar
  63. 63.
    Gibson DL, White AP, Snyder SD, Martin S, Heiss C, Azadi P, Surette M, Kay WW (2006) Salmonella produces an O-antigen capsule regulated by AgfD and important for environmental persistence. J Bacteriol 188(22):7722–7730.  https://doi.org/10.1128/JB.00809-06 CrossRefPubMedPubMedCentralGoogle Scholar
  64. 64.
    Latasa C, Roux A, Toledo-Arana A, Ghigo JM, Gamazo C, Penades JR, Lasa I (2005) BapA, a large secreted protein required for biofilm formation and host colonization of Salmonella enterica serovar Enteritidis. Mol Microbiol 58(5):1322–1339.  https://doi.org/10.1111/j.1365-2958.2005.04907.x CrossRefPubMedGoogle Scholar
  65. 65.
    Collinson SK, Emödy L, Müller KH, Trust TJ, Kay WW (1991) Purification and characterization of thin, aggregative fimbriae from Salmonella enteritidis. J Bacteriol 173(15):4773–4781CrossRefGoogle Scholar
  66. 66.
    Wang X, Rochon M, Lamprokostopoulou A, Lünsdorf H, Nimtz M, Römling U (2006) Impact of biofilm matrix components on interaction of commensal Escherichia coli with the gastrointestinal cell line HT-29. Cell Mol Life Sci 63(19–20):2352–2363.  https://doi.org/10.1007/s00018-006-6222-4 CrossRefPubMedGoogle Scholar
  67. 67.
    Monteiro C, Saxena I, Wang X, Kader A, Bokranz W, Simm R, Nobles D, Chromek M, Brauner A, Brown RM Jr, Römling U (2009) Characterization of cellulose production in Escherichia coli Nissle 1917 and its biological consequences. Environ Microbiol 11:1105–1116.  https://doi.org/10.1111/j.1462-2920.2008.01840.x CrossRefPubMedGoogle Scholar
  68. 68.
    Pontes MH, Lee EJ, Choi J, Groisman EA (2015) Salmonella promotes virulence by repressing cellulose production. Proc Natl Acad Sci USA 112(16):5183–5188.  https://doi.org/10.1073/pnas.1500989112 CrossRefPubMedGoogle Scholar
  69. 69.
    Lamprokostopoulou A, Monteiro C, Rhen M, Römling U (2010) Cyclic di-GMP signalling controls virulence properties of Salmonella enterica serovar Typhimurium at the mucosal lining. Environ Microbiol 12(1):40–53.  https://doi.org/10.1111/j.1462-2920.2009.02032.x CrossRefPubMedGoogle Scholar
  70. 70.
    Balbontin R, Vlamakis H, Kolter R (2014) Mutualistic interaction between Salmonella enterica and Aspergillus niger and its effects on Zea mays colonization. Microb Biotechnol 7(6):589–600.  https://doi.org/10.1111/1751-7915.12182 CrossRefPubMedPubMedCentralGoogle Scholar
  71. 71.
    Ellermann M, Sartor RB (2018) Intestinal bacterial biofilms modulate mucosal immune responses. J Immunol Sci 2(2):13–18CrossRefGoogle Scholar
  72. 72.
    Kai-Larsen Y, Lüthje P, Chromek M, Peters V, Wang X, Holm A, Kadas L, Hedlund KO, Johansson J, Chapman MR, Jacobson SH, Römling U, Agerberth B, Brauner A (2010) Uropathogenic Escherichia coli modulates immune responses and its curli fimbriae interact with the antimicrobial peptide LL-37. PLoS Pathog 6(7):e1001010.  https://doi.org/10.1371/journal.ppat.1001010 CrossRefPubMedPubMedCentralGoogle Scholar
  73. 73.
    Solano C, Garcia B, Valle J, Berasain C, Ghigo JM, Gamazo C, Lasa I (2002) Genetic analysis of Salmonella enteritidis biofilm formation: critical role of cellulose. Mol Microbiol 43(3):793–808CrossRefGoogle Scholar
  74. 74.
    Sun L, Vella P, Schnell R, Polyakova A, Bourenkov G, Li F, Cimdins A, Schneider TR, Lindqvist Y, Galperin MY, Schneider G, Römling U (2018) Structural and functional characterization of the BcsG subunit of the cellulose synthase in Salmonella typhimurium. J Mol Biol 430(18 Pt B):3170–3189.  https://doi.org/10.1016/j.jmb.2018.07.008 CrossRefPubMedPubMedCentralGoogle Scholar
  75. 75.
    Thongsomboon W, Serra DO, Possling A, Hadjineophytou C, Hengge R, Cegelski L (2018) Phosphoethanolamine cellulose: a naturally produced chemically modified cellulose. Science 359(6373):334–338.  https://doi.org/10.1126/science.aao4096 CrossRefGoogle Scholar
  76. 76.
    Solano C, Garcia B, Latasa C, Toledo-Arana A, Zorraquino V, Valle J, Casals J, Pedroso E, Lasa I (2009) Genetic reductionist approach for dissecting individual roles of GGDEF proteins within the c-di-GMP signaling network in Salmonella. Proc Natl Acad Sci USA 106(19):7997–8002.  https://doi.org/10.1073/pnas.0812573106 CrossRefPubMedGoogle Scholar
  77. 77.
    Ahmad I, Cimdins A, Beske T, Römling U (2017) Detailed analysis of c-di-GMP mediated regulation of csgD expression in Salmonella typhimurium. BMC Microbiol 17(1):27.  https://doi.org/10.1186/s12866-017-0934-5 CrossRefPubMedPubMedCentralGoogle Scholar
  78. 78.
    Römling U, Simm R (2009) Prevailing concepts of c-di-GMP signaling. Contrib Microbiol 16:161–181.  https://doi.org/10.1159/000219379 CrossRefPubMedGoogle Scholar
  79. 79.
    Simm R, Lusch A, Kader A, Andersson M, Römling U (2007) Role of EAL-containing proteins in multicellular behavior of Salmonella enterica serovar Typhimurium. J Bacteriol 189(9):3613–3623.  https://doi.org/10.1128/JB.01719-06 CrossRefPubMedPubMedCentralGoogle Scholar
  80. 80.
    Spurbeck RR, Alteri CJ, Himpsl SD, Mobley HL (2013) The multifunctional protein YdiV represses P fimbria-mediated adherence in uropathogenic Escherichia coli. J Bacteriol 195(14):3156–3164.  https://doi.org/10.1128/JB.02254-12 CrossRefPubMedPubMedCentralGoogle Scholar
  81. 81.
    Cimdins A, Simm R, Li F, Lüthje P, Thorell K, Sjöling A, Brauner A, Römling U (2017) Alterations of c-di-GMP turnover proteins modulate semi-constitutive rdar biofilm formation in commensal and uropathogenic Escherichia coli. Microbiology 6(5).  https://doi.org/10.1002/mbo3.508 CrossRefGoogle Scholar
  82. 82.
    Kader A, Simm R, Gerstel U, Morr M, Römling U (2006) Hierarchical involvement of various GGDEF domain proteins in rdar morphotype development of Salmonella enterica serovar Typhimurium. Mol Microbiol 60(3):602–616.  https://doi.org/10.1111/j.1365-2958.2006.05123.x CrossRefPubMedGoogle Scholar
  83. 83.
    Grantcharova N, Peters V, Monteiro C, Zakikhany K, Römling U (2010) Bistable expression of CsgD in biofilm development of Salmonella enterica serovar typhimurium. J Bacteriol 192(2):456–466.  https://doi.org/10.1128/JB.01826-08 CrossRefPubMedGoogle Scholar
  84. 84.
    MacKenzie KD, Wang Y, Shivak DJ, Wong CS, Hoffman LJ, Lam S, Kroger C, Cameron AD, Townsend HG, Köster W, White AP (2015) Bistable expression of CsgD in Salmonella enterica serovar Typhimurium connects virulence to persistence. Infect Immun 83(6):2312–2326.  https://doi.org/10.1128/IAI.00137-15 CrossRefPubMedPubMedCentralGoogle Scholar
  85. 85.
    Anwar N, Rouf SF, Römling U, Rhen M (2014) Modulation of biofilm-formation in Salmonella enterica serovar Typhimurium by the periplasmic DsbA/DsbB oxidoreductase system requires the GGDEF-EAL domain protein STM3615. PLoS One 9(8):e106095.  https://doi.org/10.1371/journal.pone.0106095 CrossRefPubMedPubMedCentralGoogle Scholar
  86. 86.
    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
  87. 87.
    Hufnagel DA, Evans ML, Greene SE, Pinkner JS, Hultgren SJ, Chapman MR (2016) The catabolite repressor protein-cyclic AMP complex regulates csgD and biofilm formation in uropathogenic Escherichia coli. J Bacteriol 198(24):3329–3334.  https://doi.org/10.1128/JB.00652-16 CrossRefPubMedPubMedCentralGoogle Scholar
  88. 88.
    Martin-Rodriguez AJ, Römling U (2017) Nucleotide second messenger signaling as a target for the control of bacterial biofilm formation. Curr Top Med Chem 17(17):1928–1944.CrossRefGoogle Scholar
  89. 89.
    Luo Y, Zhao K, Baker AE, Kuchma SL, Coggan KA, Wolfgang MC, Wong GC, O’Toole GA (2015) A hierarchical cascade of second messengers regulates Pseudomonas aeruginosa surface behaviors. MBio 6(1):e02456-14.  https://doi.org/10.1128/mBio.02456-14
  90. 90.
    Monteiro C, Papenfort K, Hentrich K, Ahmad I, Le Guyon S, Reimann R, Grantcharova N, Römling U (2012) Hfq and Hfq-dependent small RNAs are major contributors to multicellular development in Salmonella enterica serovar Typhimurium. RNA Biol 9(4):489–502.  https://doi.org/10.4161/rna.19682 CrossRefPubMedGoogle Scholar
  91. 91.
    Pratt LA, Kolter R (1998) Genetic analysis of Escherichia coli biofilm formation: roles of flagella, motility, chemotaxis and type I pili. Mol Microbiol 30(2):285–293CrossRefGoogle Scholar
  92. 92.
    Perez-Mendoza D, Sanjuan J (2016) Exploiting the commons: cyclic diguanylate regulation of bacterial exopolysaccharide production. Curr Opin Microbiol 30:36–43.  https://doi.org/10.1016/j.mib.2015.12.004 CrossRefPubMedGoogle Scholar
  93. 93.
    Bogomolnaya LM, Aldrich L, Ragoza Y, Talamantes M, Andrews KD, McClelland M, Andrews-Polymenis HL (2014) Identification of novel factors involved in modulating motility of Salmonella enterica serotype Typhimurium. PLoS One 9(11):e111513.  https://doi.org/10.1371/journal.pone.0111513 CrossRefPubMedPubMedCentralGoogle Scholar
  94. 94.
    Crepin S, Porcheron G, Houle S, Harel J, Dozois CM (2017) Altered regulation of the diguanylate cyclase YaiC reduces production of Type 1 fimbriae in a Pst mutant of uropathogenic Escherichia coli CFT073. J Bacteriol 199(24):e00168-17.  https://doi.org/10.1128/JB.00168-17
  95. 95.
    Stewart MK, Cummings LA, Johnson ML, Berezow AB, Cookson BT (2011) Regulation of phenotypic heterogeneity permits Salmonella evasion of the host caspase-1 inflammatory response. Proc Natl Acad Sci USA 108(51):20742–20747.  https://doi.org/10.1073/pnas.1108963108 CrossRefPubMedGoogle Scholar
  96. 96.
    Ahmad I, Wigren E, Le Guyon S, Vekkeli S, Blanka A, El Mouali Y, Anwar N, Chuah ML, Lünsdorf H, Frank R, Rhen M, Liang ZX, Lindqvist Y, Römling U (2013) The EAL-like protein STM1697 regulates virulence phenotypes, motility and biofilm formation in Salmonella typhimurium. Mol Microbiol 90(6):1216–1232.  https://doi.org/10.1111/mmi.12428 CrossRefPubMedGoogle Scholar
  97. 97.
    Wolfe AJ, Visick KL (2008) Get the message out: cyclic-di-GMP regulates multiple levels of flagellum-based motility. J Bacteriol 190(2):463–475.  https://doi.org/10.1128/JB.01418-07 CrossRefPubMedPubMedCentralGoogle Scholar
  98. 98.
    Chen Y, Chai Y, Guo JH, Losick R (2012) Evidence for cyclic di-GMP-mediated signaling in Bacillus subtilis. J Bacteriol 194(18):5080–5090.  https://doi.org/10.1128/JB.01092-12 CrossRefPubMedPubMedCentralGoogle Scholar
  99. 99.
    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(3):371–382.  https://doi.org/10.1006/jmbi.2000.4147 CrossRefPubMedGoogle Scholar
  100. 100.
    Pultz IS, Christen M, Kulasekara HD, Kennard A, Kulasekara B, Miller SI (2012) The response threshold of Salmonella PilZ domain proteins is determined by their binding affinities for c-di-GMP. Mol Microbiol 86(6):1424–1440.  https://doi.org/10.1111/mmi.12066 CrossRefPubMedPubMedCentralGoogle Scholar
  101. 101.
    Le Guyon S, Simm R, Rehn M, Römling U (2015) Dissecting the cyclic di-guanylate monophosphate signalling network regulating motility in Salmonella enterica serovar Typhimurium. Environ Microbiol 17(4):1310–1320.  https://doi.org/10.1111/1462-2920.12580 CrossRefPubMedGoogle Scholar
  102. 102.
    Boehm A, Kaiser M, Li H, Spangler C, Kasper CA, Ackermann M, Kaever V, Sourjik V, Roth V, Jenal U (2010) Second messenger-mediated adjustment of bacterial swimming velocity. Cell 141(1):107–116.  https://doi.org/10.1016/j.cell.2010.01.018 CrossRefGoogle Scholar
  103. 103.
    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(1):128–139.  https://doi.org/10.1016/j.molcel.2010.03.001 CrossRefPubMedPubMedCentralGoogle Scholar
  104. 104.
    Fang X, Gomelsky M (2010) A post-translational, c-di-GMP-dependent mechanism regulating flagellar motility. Mol Microbiol 76(5):1295–1305.  https://doi.org/10.1111/j.1365-2958.2010.07179.x CrossRefGoogle Scholar
  105. 105.
    Zorraquino V, Garcia B, Latasa C, Echeverz M, Toledo-Arana A, Valle J, Lasa I, Solano C (2013) Coordinated cyclic-di-GMP repression of Salmonella motility through YcgR and cellulose. J Bacteriol 195(3):417–428.  https://doi.org/10.1128/JB.01789-12 CrossRefPubMedPubMedCentralGoogle Scholar
  106. 106.
    Takaya A, Erhardt M, Karata K, Winterberg K, Yamamoto T, Hughes KT (2012) YdiV: a dual function protein that targets FlhDC for ClpXP-dependent degradation by promoting release of DNA-bound FlhDC complex. Mol Microbiol 83(6):1268–1284.  https://doi.org/10.1111/j.1365-2958.2012.08007.x CrossRefPubMedPubMedCentralGoogle Scholar
  107. 107.
    Hisert KB, MacCoss M, Shiloh MU, Darwin KH, Singh S, Jones RA, Ehrt S, Zhang Z, Gaffney BL, Gandotra S, Holden DW, Murray D, Nathan C (2005) A glutamate-alanine-leucine (EAL) domain protein of Salmonella controls bacterial survival in mice, antioxidant defence and killing of macrophages: role of cyclic diGMP. Mol Microbiol 56(5):1234–1245.  https://doi.org/10.1111/j.1365-2958.2005.04632.x CrossRefPubMedGoogle Scholar
  108. 108.
    Spöring I, Felgner S, Preusse M, Eckweiler D, Rohde M, Häussler S, Weiss S, Erhardt M (2018) Regulation of flagellum biosynthesis in response to cell envelope stress in Salmonella enterica serovar Typhimurium. MBio 9(3):e00736-17.  https://doi.org/10.1128/mBio.00736-17
  109. 109.
    Jonas K, Edwards AN, Ahmad I, Romeo T, Römling U, Melefors Ö (2010) Complex regulatory network encompassing the Csr, c-di-GMP and motility systems of Salmonella typhimurium. Environ Microbiol 12(2):524–540.  https://doi.org/10.1111/j.1462-2920.2009.02097.x CrossRefPubMedGoogle Scholar
  110. 110.
    Harshey RM, Matsuyama T (1994) Dimorphic transition in Escherichia coli and Salmonella typhimurium: surface-induced differentiation into hyperflagellate swarmer cells. Proc Natl Acad Sci USA 91(18):8631–8635.  https://doi.org/10.1073/pnas.91.18.8631 CrossRefPubMedGoogle Scholar
  111. 111.
    Bontemps-Gallo S, Bohin JP, Lacroix JM (2017) Osmoregulated periplasmic glucans. EcoSal Plus 7(2).  https://doi.org/10.1128/ecosalplus.ESP-0001-2017
  112. 112.
    Bhagwat AA, Young L, Smith AD, Bhagwat M (2017) Transcriptomic analysis of the swarm motility phenotype of Salmonella enterica serovar Typhimurium mutant defective in periplasmic glucan synthesis. Curr Microbiol 74(9):1005–1014.  https://doi.org/10.1007/s00284-017-1267-1 CrossRefPubMedGoogle Scholar
  113. 113.
    Jonas K, Edwards AN, Simm R, Romeo T, Römling U, Melefors Ö (2008) The RNA binding protein CsrA controls cyclic di-GMP metabolism by directly regulating the expression of GGDEF proteins. Mol Microbiol 70(1):236–257.  https://doi.org/10.1111/j.1365-2958.2008.06411.x CrossRefPubMedPubMedCentralGoogle Scholar
  114. 114.
    Kulasakara H, Lee V, Brencic A, Liberati N, Urbach J, Miyata S, Lee DG, Neely AN, Hyodo M, Hayakawa Y, Ausubel FM, Lory S (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(8):2839–2844.  https://doi.org/10.1073/pnas.0511090103 CrossRefGoogle Scholar
  115. 115.
    Römling U (2012) Cyclic di-GMP, an established secondary messenger still speeding up. Environ Microbiol 14(8):1817–1829.  https://doi.org/10.1111/j.1462-2920.2011.02617.x CrossRefPubMedGoogle Scholar
  116. 116.
    Engl C, Waite CJ, McKenna JF, Bennett MH, Hamann T, Buck M (2014) Chp8, a diguanylate cyclase from Pseudomonas syringae pv. Tomato DC3000, suppresses the pathogen-associated molecular pattern flagellin, increases extracellular polysaccharides, and promotes plant immune evasion. MBio 5(3):e01168-14.  https://doi.org/10.1128/mBio.01168-14 CrossRefPubMedPubMedCentralGoogle Scholar
  117. 117.
    De Wit S, Taelman H, Van de Perre P, Rouvroy D, Clumeck N (1988) Salmonella bacteremia in African patients with human immunodeficiency virus infection. Eur J Clin Microbiol Infect Dis 7(1):45–47CrossRefGoogle Scholar
  118. 118.
    Tsolis RM, Xavier MN, Santos RL, Bäumler AJ (2011) How to become a top model: impact of animal experimentation on human Salmonella disease research. Infect Immun 79(5):1806–1814.  https://doi.org/10.1128/IAI.01369-10 CrossRefPubMedPubMedCentralGoogle Scholar
  119. 119.
    Tamayo R, Pratt JT, Camilli A (2007) Roles of cyclic diguanylate in the regulation of bacterial pathogenesis. Annu Rev Microbiol 61:131–148.  https://doi.org/10.1146/annurev.micro.61.080706.093426 CrossRefPubMedPubMedCentralGoogle Scholar
  120. 120.
    Zheng Y, Sambou T, Bogomolnaya LM, Cirillo JD, McClelland M, Andrews-Polymenis H (2013) The EAL domain containing protein STM2215 (rtn) is needed during Salmonella infection and has cyclic di-GMP phosphodiesterase activity. Mol Microbiol 89(3):403–419.  https://doi.org/10.1111/mmi.12284 CrossRefPubMedGoogle Scholar
  121. 121.
    Amarasinghe JJ, D’Hondt RE, Waters CM, Mantis NJ (2013) Exposure of Salmonella enterica serovar Typhimurium to a protective monoclonal IgA triggers exopolysaccharide production via a diguanylate cyclase-dependent pathway. Infect Immun 81(3):653–664.  https://doi.org/10.1128/IAI.00813-12 CrossRefPubMedPubMedCentralGoogle Scholar
  122. 122.
    Gogoi M, Shreenivas MM, Chakravortty D (2019) Hoodwinking the big-eater to prosper: the Salmonella-macrophage paradigm. J Innate Immun 11(3):289–299.  https://doi.org/10.1159/000490953 CrossRefPubMedGoogle Scholar
  123. 123.
    Rhen M (2019) Salmonella and reactive oxygen species: a love-hate relationship. J Innate Immun 11(3):216–226.  https://doi.org/10.1159/000496370 CrossRefPubMedPubMedCentralGoogle Scholar
  124. 124.
    Fields PI, Swanson RV, Haidaris CG, Heffron F (1986) Mutants of Salmonella typhimurium that cannot survive within the macrophage are avirulent. Proc Natl Acad Sci USA 83(14):5189–5193.  https://doi.org/10.1073/pnas.83.14.5189 CrossRefPubMedGoogle Scholar
  125. 125.
    Ahmad I, Rouf SF, Sun L, Cimdins A, Shafeeq S, Le Guyon S, Schottkowski M, Rhen M, Römling U (2016) BcsZ inhibits biofilm phenotypes and promotes virulence by blocking cellulose production in Salmonella enterica serovar Typhimurium. Microb Cell Factories 15(1):177.  https://doi.org/10.1186/s12934-016-0576-6 CrossRefGoogle Scholar
  126. 126.
    Petersen E, Mills E, Miller SI (2019) Cyclic-di-GMP regulation promotes survival of a slow-replicating subpopulation of intracellular Salmonella Typhimurium. Proc Natl Acad Sci USA 116(13):6335–6340.  https://doi.org/10.1073/pnas.1901051116 CrossRefPubMedGoogle Scholar
  127. 127.
    Yaron S, Römling U (2014) Biofilm formation by enteric pathogens and its role in plant colonization and persistence. Microb Biotechnol 7(6):496–516.  https://doi.org/10.1111/1751-7915.12186 CrossRefPubMedPubMedCentralGoogle Scholar
  128. 128.
    Barak JD, Jahn CE, Gibson DL, Charkowski AO (2007) The role of cellulose and O-antigen capsule in the colonization of plants by Salmonella enterica. Mol Plant-Microbe Interact 20(9):1083–1091.  https://doi.org/10.1094/MPMI-20-9-1083 CrossRefPubMedGoogle Scholar
  129. 129.
    Römling U, Galperin MY (2015) Bacterial cellulose biosynthesis: diversity of operons, subunits, products, and functions. Trends Microbiol 23:545–557.  https://doi.org/10.1016/j.tim.2015.05.005 CrossRefPubMedPubMedCentralGoogle Scholar
  130. 130.
    White AP, Gibson DL, Kim W, Kay WW, Surette MG (2006) Thin aggregative fimbriae and cellulose enhance long-term survival and persistence of Salmonella. J Bacteriol 188(9):3219–3227.  https://doi.org/10.1128/JB.188.9.3219-3227.2006 CrossRefPubMedPubMedCentralGoogle Scholar
  131. 131.
    Gerstel U, Römling U (2001) Oxygen tension and nutrient starvation are major signals that regulate agfD promoter activity and expression of the multicellular morphotype in Salmonella typhimurium. Environ Microbiol 3(10):638–648CrossRefGoogle Scholar
  132. 132.
    Scher K, Römling U, Yaron S (2005) Effect of heat, acidification, and chlorination on Salmonella enterica serovar Typhimurium cells in a biofilm formed at the air-liquid interface. Appl Environ Microbiol 71(3):1163–1168.  https://doi.org/10.1128/AEM.71.3.1163-1168.2005 CrossRefPubMedPubMedCentralGoogle Scholar
  133. 133.
    Tabak M, Scher K, Hartog E, Römling U, Matthews KR, Chikindas ML, Yaron S (2007) Effect of triclosan on Salmonella typhimurium at different growth stages and in biofilms. FEMS Microbiol Lett 267(2):200–206.  https://doi.org/10.1111/j.1574-6968.2006.00547.x CrossRefPubMedGoogle Scholar
  134. 134.
    Ramachandran G, Aheto K, Shirtliff ME, Tennant SM (2016) Poor biofilm-forming ability and long-term survival of invasive Salmonella Typhimurium ST313. Pathog Dis 74(5).  https://doi.org/10.1093/femspd/ftw049 CrossRefGoogle Scholar
  135. 135.
    Singletary LA, Karlinsey JE, Libby SJ, Mooney JP, Lokken KL, Tsolis RM, Byndloss MX, Hirao LA, Gaulke CA, Crawford RW, Dandekar S, Kingsley RA, Msefula CL, Heyderman RS, Fang FC (2016) Loss of multicellular behavior in epidemic African nontyphoidal Salmonella enterica serovar Typhimurium ST313 strain D23580. mBio 7(2):e02265.  https://doi.org/10.1128/mBio.02265-15 CrossRefPubMedPubMedCentralGoogle Scholar
  136. 136.
    Povolotsky TL, Hengge R (2015) Genome-based comparison of c-di-GMP signaling in pathogenic and commensal Escherichia coli strains. J Bacteriol 198:111–126.  https://doi.org/10.1128/JB.00520-15 CrossRefPubMedPubMedCentralGoogle Scholar
  137. 137.
    Hengge R, Galperin MY, Ghigo JM, Gomelsky M, Green J, Hughes KT, Jenal U, Landini P (2016) Systematic nomenclature for GGDEF and EAL domain-containing cyclic di-GMP turnover proteins of Escherichia coli. J Bacteriol 198(1):7–11.  https://doi.org/10.1128/JB.00424-15 CrossRefPubMedGoogle Scholar
  138. 138.
    Zähringer F, Lacanna E, Jenal U, Schirmer T, Boehm A (2013) Structure and signaling mechanism of a zinc-sensory diguanylate cyclase. Structure 21(7):1149–1157.  https://doi.org/10.1016/j.str.2013.04.026 CrossRefPubMedGoogle Scholar
  139. 139.
    Tschowri N, Busse S, Hengge R (2009) The BLUF-EAL protein YcgF acts as a direct anti-repressor in a blue-light response of Escherichia coli. Genes Dev 23(4):522–534.  https://doi.org/10.1101/gad.499409 CrossRefPubMedPubMedCentralGoogle Scholar
  140. 140.
    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(14):4774–4781.  https://doi.org/10.1128/JB.187.14.4774-4781.2005 CrossRefPubMedPubMedCentralGoogle Scholar
  141. 141.
    Blount ZD (2015) The unexhausted potential of E. coli. Elife 4:e05826.  https://doi.org/10.7554/eLife.05826 CrossRefPubMedCentralGoogle Scholar
  142. 142.
    Povolotsky TL, Hengge R (2016) Genome-based comparison of cyclic di-GMP signaling in pathogenic and commensal Escherichia coli strains. J Bacteriol 198(1):111–126.  https://doi.org/10.1128/JB.00520-15 CrossRefPubMedGoogle Scholar
  143. 143.
    Zlatkov N, Uhlin BE (2019) Absence of global stress regulation in Escherichia coli promotes pathoadaptation and novel c-di-GMP-dependent metabolic capability. Sci Rep 9(1):2600.  https://doi.org/10.1038/s41598-019-39580-w CrossRefPubMedPubMedCentralGoogle Scholar
  144. 144.
    Richter AM, Povolotsky TL, Wieler LH, Hengge R (2014) Cyclic-di-GMP signalling and biofilm-related properties of the Shiga toxin-producing 2011 German outbreak Escherichia coli O104:H4. EMBO Mol Med 6(12):1622–1637.  https://doi.org/10.15252/emmm.201404309 CrossRefPubMedPubMedCentralGoogle Scholar
  145. 145.
    Whiteley AT, Eaglesham JB, de Oliveira Mann CC, Morehouse BR, Lowey B, Nieminen EA, Danilchanka O, King DS, Lee ASY, Mekalanos JJ, Kranzusch PJ (2019) Bacterial cGAS-like enzymes synthesize diverse nucleotide signals. Nature 566:259–263.  https://doi.org/10.1038/s41586-019-0953-5 CrossRefGoogle Scholar
  146. 146.
    Li F, Cimdins A, Rohde M, Jänsch L, Kaever V, Nimtz M, Römling U (2019) DncV synthesizes cyclic GAMP and regulates biofilm formation and motility in Escherichia coli ECOR31. mBio 10(2):e02492-18Google Scholar
  147. 147.
    Cohen D, Melamed S, Millman A, Shulman G, Oppenheimer-Shaanan Y, Kacen A, Doron S, Amitai G, Sorek R (2019) Cyclic GMP-AMP signalling protects bacteria against viral infection. Nature 574(7780):691–695.  https://doi.org/10.1038/s41586-019-1605-5 CrossRefGoogle Scholar
  148. 148.
    Davies BW, Bogard RW, Young TS, Mekalanos JJ (2012) Coordinated regulation of accessory genetic elements produces cyclic di-nucleotides for V. cholerae virulence. Cell 149(2):358–370.  https://doi.org/10.1016/j.cell.2012.01.053 CrossRefPubMedPubMedCentralGoogle Scholar
  149. 149.
    Waldron EJ, Snyder D, Fernandez NL, Sileo E, Inoyama D, Freundlich JS, Waters CM, Cooper VS, Neiditch MB (2019) Structural basis of DSF recognition by its receptor RpfR and its regulatory interaction with the DSF synthase RpfF. PLoS Biol 17(2):e3000123.  https://doi.org/10.1371/journal.pbio.3000123 CrossRefPubMedPubMedCentralGoogle Scholar
  150. 150.
    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(4):995–1007.  https://doi.org/10.1111/j.1365-2958.2006.05568.x CrossRefPubMedGoogle Scholar
  151. 151.
    Lind PA, Farr AD, Rainey PB (2015) Experimental evolution reveals hidden diversity in evolutionary pathways. Elife 4:e07074.  https://doi.org/10.7554/eLife.07074 CrossRefPubMedCentralGoogle Scholar
  152. 152.
    Traverse CC, Mayo-Smith LM, Poltak SR, Cooper VS (2013) Tangled bank of experimentally evolved Burkholderia biofilms reflects selection during chronic infections. Proc Natl Acad Sci USA 110(3):E250–E259.  https://doi.org/10.1073/pnas.1207025110 CrossRefPubMedGoogle Scholar
  153. 153.
    Reinders A, Hee CS, Ozaki S, Mazur A, Boehm A, Schirmer T, Jenal U (2016) Expression and genetic activation of cyclic di-GMP-specific phosphodiesterases in Escherichia coli. J Bacteriol 198(3):448–462.  https://doi.org/10.1128/JB.00604-15 CrossRefPubMedPubMedCentralGoogle Scholar
  154. 154.
    Muriel C, Blanco-Romero E, Trampari E, Arrebola E, Duran D, Redondo-Nieto M, Malone JG, Martin M, Rivilla R (2019) The diguanylate cyclase AdrA regulates flagellar biosynthesis in Pseudomonas fluorescens F113 through SadB. Sci Rep 9(1):8096.  https://doi.org/10.1038/s41598-019-44554-z CrossRefPubMedPubMedCentralGoogle Scholar
  155. 155.
    Deng Y, Schmid N, Wang C, Wang J, Pessi G, Wu D, Lee J, Aguilar C, Ahrens CH, Chang C, Song H, Eberl L, Zhang LH (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(38):15479–15484.  https://doi.org/10.1073/pnas.1205037109 CrossRefPubMedGoogle Scholar
  156. 156.
    Robert X, Gouet P (2014) Deciphering key features in protein structures with the new ENDscript server. Nucleic Acids Res 42(Web Server issue):W320–W324.  https://doi.org/10.1093/nar/gku316 CrossRefPubMedPubMedCentralGoogle Scholar

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© Springer Nature Switzerland AG 2020

Authors and Affiliations

  1. 1.Department of Microbiology, Tumor and Cell BiologyKarolinska InstitutetStockholmSweden

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