Skip to main content
SpringerLink
Log in
Book cover

Microbial Cyclic Di-Nucleotide Signaling pp 487–517Cite as

Unconventional Cyclic di-GMP Signaling in Escherichia coli

  • Chapter
  • First Online:

Abstract

The species Escherichia coli represents an unfathomable variety of commensal, pathogenic, and environmental strains. The conventional cyclic di-GMP signaling in E. coli controls sessility-motility changes linked to commensalism and/or pathogenicity. Extraintestinal Pathogenic E. coli (ExPEC) are “commensals” that can cause an array of infections outside the gastrointestinal tract. To accommodate their pathogenic lifestyle with the commensal one, ExPEC biology is shaped not only by the presence of specific virulence genes and pathoadaptive mutations but also by regulatory adaptations. Bioinformatic and genetic studies indicate that the cyclic di-GMP signaling network is included in the adaptation process. For example, some neuroinvasive ExPEC were found to maintain reduced cyclic di-GMP levels due to RpoS deactivation, resulting in loss of appearance of the rugose morphotype. Moreover, ExPEC has a diversified repertoire of cyclic di-GMP degrading enzymes obtained by acquisition of novel genes often associated with fimbrial biogenesis gene clusters (e.g., sfaY/papY/focY) and by modification or deletion of specific core genome genes. For example, the majority of ExPEC contains a shortened allelic variant of the ycgG gene and some ExPEC strains do not even carry the genetic locus. New combinations of regulators offer a new cyclic di-GMP platform for S-fimbrial biogenesis and for new metabolic capabilities leading to citrate utilization and ferric citrate uptake. In this review, we outline the prerequisites for the unconventional signaling network, the rationale behind its existence in ExPEC, and future perspectives in studies of ExPEC.

This is a preview of subscription content, 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

Learn about institutional subscriptions

References

  1. Lawrence JG, Ochman H (1998) Molecular archaeology of the Escherichia coli genome. Proc Natl Acad Sci U S A 95(16):9413–9417

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Ochman H, Wilson AC (1987) Evolution in bacteria: evidence for a universal substitution rate in cellular genomes. J Mol Evol 26(1–2):74–86

    Article  CAS  PubMed  Google Scholar 

  3. Luo ZX, Yuan CX, Meng QJ, Ji Q (2011) A Jurassic eutherian mammal and divergence of marsupials and placentals. Nature 476(7361):442–445. https://doi.org/10.1038/nature10291

    Article  CAS  PubMed  Google Scholar 

  4. Tenaillon O, Skurnik D, Picard B, Denamur E (2010) The population genetics of commensal Escherichia coli. Nat Rev Microbiol 8(3):207–217. https://doi.org/10.1038/nrmicro2298

    Article  CAS  PubMed  Google Scholar 

  5. Ochman H, Jones IB (2000) Evolutionary dynamics of full genome content in Escherichia coli. EMBO J 19(24):6637–6643. https://doi.org/10.1093/emboj/19.24.6637

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Strockbine FSN (2005) Escherichia. Bergey’s manual of systematic bacteriology, 2nd edn. Springer, New York

    Google Scholar 

  7. Gordon DM, Cowling A (2003) The distribution and genetic structure of Escherichia coli in Australian vertebrates: host and geographic effects. Microbiology 149(Pt 12):3575–3586. https://doi.org/10.1099/mic.0.26486-0

    Article  CAS  PubMed  Google Scholar 

  8. Donnenberg MS (2013) Escherichia coli: pathotypes and principles of pathogenesis, 2nd edn. Academic, Amsterdam

    Google Scholar 

  9. Szunerits S, Zagorodko O, Cogez V, Dumych T, Chalopin T, Alvarez Dorta D, Sivignon A, Barnich N, Harduin-Lepers A, Larroulet I, Yanguas Serrano A, Siriwardena A, Pesquera A, Zurutuza A, Gouin SG, Boukherroub R, Bouckaert J (2016) Differentiation of Crohn’s disease-associated isolates from other pathogenic Escherichia coli by fimbrial adhesion under shear force. Biology (Basel) 5(2):14. https://doi.org/10.3390/biology5020014

    Article  PubMed Central  CAS  Google Scholar 

  10. Croxen MA, Finlay BB (2010) Molecular mechanisms of Escherichia coli pathogenicity. Nat Rev Microbiol 8(1):26–38. https://doi.org/10.1038/nrmicro2265

    Article  CAS  PubMed  Google Scholar 

  11. Tozzoli R, Sheutz F (2014) Diarrhoeagenic Escherichia coli infections in humans. In: Morabito S (ed) Pathogenic Escherichia coli. Caister Academic Press, Norfolk

    Google Scholar 

  12. Mainil J, Fairbrother J (2014) Pathogenic Escherichia coli in domestic mammals and birds. In: Morabito S (ed) Pathogenic Escherichia coli. Caister Academic Press, Norfolk

    Google Scholar 

  13. Kaper JB, Nataro JP, Mobley HL (2004) Pathogenic Escherichia coli. Nat Rev Microbiol 2(2):123–140. https://doi.org/10.1038/nrmicro818

    Article  CAS  PubMed  Google Scholar 

  14. Nataro JP, Kaper JB (1998) Diarrheagenic Escherichia coli. Clin Microbiol Rev 11(1):142–201

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Boudeau J, Glasser AL, Masseret E, Joly B, Darfeuille-Michaud A (1999) Invasive ability of an Escherichia coli strain isolated from the ileal mucosa of a patient with Crohn’s disease. Infect Immun 67(9):4499–4509

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Glasser AL, Boudeau J, Barnich N, Perruchot MH, Colombel JF, Darfeuille-Michaud A (2001) Adherent invasive Escherichia coli strains from patients with Crohn’s disease survive and replicate within macrophages without inducing host cell death. Infect Immun 69(9):5529–5537

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Selander RK, Caugant DA, Ochman H, Musser JM, Gilmour MN, Whittam TS (1986) Methods of multilocus enzyme electrophoresis for bacterial population genetics and systematics. Appl Environ Microbiol 51(5):873–884

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Goullet P, Picard B (1989) Comparative electrophoretic polymorphism of esterases and other enzymes in Escherichia coli. J Gen Microbiol 135(1):135–143. https://doi.org/10.1099/00221287-135-1-135

    Article  CAS  PubMed  Google Scholar 

  19. Neidhardt FC, Curtiss R (1996) Escherichia coli and Salmonella: cellular and molecular biology, 2nd edn. ASM, Washington, DC

    Google Scholar 

  20. Touchon M, Hoede C, Tenaillon O, Barbe V, Baeriswyl S, Bidet P, Bingen E, Bonacorsi S, Bouchier C, Bouvet O, Calteau A, Chiapello H, Clermont O, Cruveiller S, Danchin A, Diard M, Dossat C, Karoui ME, Frapy E, Garry L, Ghigo JM, Gilles AM, Johnson J, Le Bouguenec C, Lescat M, Mangenot S, Martinez-Jehanne V, Matic I, Nassif X, Oztas S, Petit MA, Pichon C, Rouy Z, Ruf CS, Schneider D, Tourret J, Vacherie B, Vallenet D, Medigue C, Rocha EP, Denamur E (2009) Organised genome dynamics in the Escherichia coli species results in highly diverse adaptive paths. PLoS Genet 5(1):e1000344. https://doi.org/10.1371/journal.pgen.1000344

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Vila J, Saez-Lopez E, Johnson JR, Romling U, Dobrindt U, Canton R, Giske CG, Naas T, Carattoli A, Martinez-Medina M, Bosch J, Retamar P, Rodriguez-Bano J, Baquero F, Soto SM (2016) Escherichia coli: an old friend with new tidings. FEMS Microbiol Rev 40(4):437–463. https://doi.org/10.1093/femsre/fuw005

    Article  CAS  PubMed  Google Scholar 

  22. Dobrindt U, Chowdary MG, Krumbholz G, Hacker J (2010) Genome dynamics and its impact on evolution of Escherichia coli. Med Microbiol Immunol 199(3):145–154. https://doi.org/10.1007/s00430-010-0161-2

    Article  CAS  PubMed  Google Scholar 

  23. Subashchandrabose S, Mobley HL (2015) Virulence and fitness determinants of uropathogenic Escherichia coli. Microbiol Spectr 3(4). https://doi.org/10.1128/microbiolspec.UTI-0015-2012

  24. Kucheria R, Dasgupta P, Sacks SH, Khan MS, Sheerin NS (2005) Urinary tract infections: new insights into a common problem. Postgrad Med J 81(952):83–86. https://doi.org/10.1136/pgmj.2004.023036

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Foxman B, Manning SD, Tallman P, Bauer R, Zhang L, Koopman JS, Gillespie B, Sobel JD, Marrs CF (2002) Uropathogenic Escherichia coli are more likely than commensal E. coli to be shared between heterosexual sex partners. Am J Epidemiol 156(12):1133–1140

    Article  PubMed  Google Scholar 

  26. Marrs CF, Zhang L, Foxman B (2005) Escherichia coli mediated urinary tract infections: are there distinct uropathogenic E. coli (UPEC) pathotypes? FEMS Microbiol Lett 252(2):183–190. https://doi.org/10.1016/j.femsle.2005.08.028

    Article  CAS  PubMed  Google Scholar 

  27. Agrawal S, Nadel S (2011) Acute bacterial meningitis in infants and children: epidemiology and management. Paediatr Drugs 13(6):385–400. https://doi.org/10.2165/11593340-000000000-00000

    Article  PubMed  Google Scholar 

  28. Gaschignard J, Levy C, Romain O, Cohen R, Bingen E, Aujard Y, Boileau P (2011) Neonatal bacterial meningitis: 444 cases in 7 years. Pediatr Infect Dis J 30(3):212–217

    Article  PubMed  Google Scholar 

  29. Saez-Llorens X, McCracken GH Jr (2003) Bacterial meningitis in children. Lancet 361(9375):2139–2148. https://doi.org/10.1016/S0140-6736(03)13693-8

    Article  PubMed  Google Scholar 

  30. McCracken GH Jr, Sarff LD, Glode MP, Mize SG, Schiffer MS, Robbins JB, Gotschlich EC, Orskov I, Orskov F (1974) Relation between Escherichia coli K1 capsular polysaccharide antigen and clinical outcome in neonatal meningitis. Lancet 2(7875):246–250

    Article  PubMed  Google Scholar 

  31. Stoll BJ, Hansen N, Fanaroff AA, Wright LL, Carlo WA, Ehrenkranz RA, Lemons JA, Donovan EF, Stark AR, Tyson JE, Oh W, Bauer CR, Korones SB, Shankaran S, Laptook AR, Stevenson DK, Papile LA, Poole WK (2002) Changes in pathogens causing early-onset sepsis in very-low-birth-weight infants. N Engl J Med 347(4):240–247. https://doi.org/10.1056/NEJMoa012657

    Article  PubMed  Google Scholar 

  32. Barichello T, Dagostim VS, Generoso JS, Simões LR, Dominguini D, Silvestre C, Michels M, Vilela MC, Jornada LK, Comim CM, Dal-Pizzol F, Teixeira AL, Quevedo J (2014) Neonatal Escherichia coli K1 meningitis causes learning and memory impairments in adulthood. J Neuroimmunol 272(1–2):35–41. https://doi.org/10.1016/j.jneuroim.2014.05.003

    Article  CAS  PubMed  Google Scholar 

  33. Doran KS, Fulde M, Gratz N, Kim BJ, Nau R, Prasadarao N, Schubert-Unkmeir A, Tuomanen EI, Valentin-Weigand P (2016) Host-pathogen interactions in bacterial meningitis. Acta Neuropathol 131(2):185–209. https://doi.org/10.1007/s00401-015-1531-z

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Bonacorsi S, Bingen E (2005) Molecular epidemiology of Escherichia coli causing neonatal meningitis. Int J Med Microbiol 295(6–7):373–381. https://doi.org/10.1016/j.ijmm.2005.07.011

    Article  CAS  PubMed  Google Scholar 

  35. Xie Y, Kim KJ, Kim KS (2004) Current concepts on Escherichia coli K1 translocation of the blood-brain barrier. FEMS Immunol Med Microbiol 42(3):271–279. https://doi.org/10.1016/j.femsim.2004.09.001

    Article  CAS  PubMed  Google Scholar 

  36. Mayor-Lynn K, Gonzalez-Quintero VH, O’Sullivan MJ, Hartstein AI, Roger S, Tamayo M (2005) Comparison of early-onset neonatal sepsis caused by Escherichia coli and group B Streptococcus. Am J Obstet Gynecol 192(5):1437–1439. https://doi.org/10.1016/j.ajog.2004.12.031

    Article  PubMed  Google Scholar 

  37. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Evans DJ, Evans DG, Höhne C, Noble MA, Haldane EV, Lior H, Young LS (1981) Hemolysin and K antigens in relation to serotype and hemagglutination type of Escherichia coli isolated from extraintestinal infections. J Clin Microbiol 13(1):171–178

    Article  PubMed  PubMed Central  Google Scholar 

  39. Korhonen TK, Valtonen MV, Parkkinen J, Väisänen-Rhen V, Finne J, Orskov F, Orskov I, Svenson SB, Mäkelä PH (1985) Serotypes, hemolysin production, and receptor recognition of Escherichia coli strains associated with neonatal sepsis and meningitis. Infect Immun 48(2):486–491

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Landraud L, Gauthier M, Fosse T, Boquet P (2000) Frequency of Escherichia coli strains producing the cytotoxic necrotizing factor (CNF1) in nosocomial urinary tract infections. Lett Appl Microbiol 30(3):213–216

    Article  CAS  PubMed  Google Scholar 

  41. Khan NA, Wang Y, Kim KJ, Chung JW, Wass CA, Kim KS (2002) Cytotoxic necrotizing factor-1 contributes to Escherichia coli K1 invasion of the central nervous system. J Biol Chem 277(18):15607–15612. https://doi.org/10.1074/jbc.M112224200

    Article  CAS  PubMed  Google Scholar 

  42. Pascal TA, Abrol R, Mittal R, Wang Y, Prasadarao NV, Goddard WA (2010) Experimental validation of the predicted binding site of Escherichia coli K1 outer membrane protein a to human brain microvascular endothelial cells: identification of critical mutations that prevent E. coli meningitis. J Biol Chem 285(48):37753–37761. https://doi.org/10.1074/jbc.M110.122804

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Prasadarao NV (2002) Identification of Escherichia coli outer membrane protein a receptor on human brain microvascular endothelial cells. Infect Immun 70(8):4556–4563

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Mittal R, Prasadarao NV (2011) gp96 expression in neutrophils is critical for the onset of Escherichia coli K1 (RS218) meningitis. Nat Commun 2:552. https://doi.org/10.1038/ncomms1554

    Article  CAS  PubMed  Google Scholar 

  45. Huang SH, Chen YH, Kong G, Chen SH, Besemer J, Borodovsky M, Jong A (2001) A novel genetic island of meningitic Escherichia coli K1 containing the ibeA invasion gene (GimA): functional annotation and carbon-source-regulated invasion of human brain microvascular endothelial cells. Funct Integr Genomics 1(5):312–322. https://doi.org/10.1007/s101420100039

    Article  CAS  PubMed  Google Scholar 

  46. Huang SH, Wass C, Fu Q, Prasadarao NV, Stins M, Kim KS (1995) Escherichia coli invasion of brain microvascular endothelial cells in vitro and in vivo: molecular cloning and characterization of invasion gene ibe10. Infect Immun 63(11):4470–4475

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Prasadarao NV, Wass CA, Huang SH, Kim KS (1999) Identification and characterization of a novel Ibe10 binding protein that contributes to Escherichia coli invasion of brain microvascular endothelial cells. Infect Immun 67(3):1131–1138

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Bloch CA, Huang SH, Rode CK, Kim KS (1996) Mapping of noninvasion TnphoA mutations on the Escherichia coli O18:K1:H7 chromosome. FEMS Microbiol Lett 144(2–3):171–176

    Article  CAS  PubMed  Google Scholar 

  49. Silver RP, Aaronson W, Vann WF (1988) The K1 capsular polysaccharide of Escherichia coli. Rev Infect Dis 10(Suppl. 2):S282–S286

    Article  CAS  PubMed  Google Scholar 

  50. Jann B, Jann K (1990) Structure and biosynthesis of the capsular antigens of Escherichia coli. Curr Top Microbiol Immunol 150:19–42

    CAS  PubMed  Google Scholar 

  51. Jann K, Jann B (1987) Polysaccharide antigens of Escherichia coli. Rev Infect Dis 9(Suppl. 5):S517–S526

    Article  CAS  PubMed  Google Scholar 

  52. Robbins JB, McCracken GH, Gotschlich EC, Orskov F, Orskov I, Hanson LA (1974) Escherichia coli K1 capsular polysaccharide associated with neonatal meningitis. N Engl J Med 290(22):1216–1220. https://doi.org/10.1056/NEJM197405302902202

    Article  CAS  PubMed  Google Scholar 

  53. Mobley HL, Donnenberg MS, Hagan EC (2009) Uropathogenic Escherichia coli. EcoSal Plus 3(2):678–687. https://doi.org/10.1128/ecosalplus.8.6.1.3

    Article  CAS  Google Scholar 

  54. 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

    Article  CAS  PubMed  Google Scholar 

  55. 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

    Article  CAS  PubMed  Google Scholar 

  56. Hengge R (2009) Principles of c-di-GMP signalling in bacteria. Nat Rev Microbiol 7(4):263–273. https://doi.org/10.1038/nrmicro2109

    Article  CAS  PubMed  Google Scholar 

  57. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. 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):163–167

    Article  CAS  PubMed  Google Scholar 

  60. 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

    Article  CAS  PubMed  Google Scholar 

  61. Povolotsky TL, Hengge R (2015) 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

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  62. Tuckerman JR, Gonzalez G, Gilles-Gonzalez MA (2011) Cyclic di-GMP activation of polynucleotide phosphorylase signal-dependent RNA processing. J Mol Biol 407(5):633–639. https://doi.org/10.1016/j.jmb.2011.02.019

    Article  CAS  PubMed  Google Scholar 

  63. Tuckerman JR, Gonzalez G, Sousa EH, Wan X, Saito JA, Alam M, Gilles-Gonzalez MA (2009) An oxygen-sensing diguanylate cyclase and phosphodiesterase couple for c-di-GMP control. Biochemistry 48(41):9764–9774. https://doi.org/10.1021/bi901409g

    Article  CAS  PubMed  Google Scholar 

  64. 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

    Article  CAS  PubMed  Google Scholar 

  65. 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

    Article  CAS  PubMed  Google Scholar 

  66. Schirmer T, Jenal U (2009) Structural and mechanistic determinants of c-di-GMP signalling. Nat Rev Microbiol 7(10):724–735. https://doi.org/10.1038/nrmicro2203

    Article  CAS  PubMed  Google Scholar 

  67. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  68. Suzuki K, Babitzke P, Kushner SR, Romeo T (2006) Identification of a novel regulatory protein (CsrD) that targets the global regulatory RNAs CsrB and CsrC for degradation by RNase E. Genes Dev 20(18):2605–2617. https://doi.org/10.1101/gad.1461606

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  69. Vakulskas CA, Leng Y, Abe H, Amaki T, Okayama A, Babitzke P, Suzuki K, Romeo T (2016) Antagonistic control of the turnover pathway for the global regulatory sRNA CsrB by the CsrA and CsrD proteins. Nucleic Acids Res 44(16):7896–7910. https://doi.org/10.1093/nar/gkw484

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  70. Zakikhany K, Harrington CR, Nimtz M, Hinton JC, Romling U (2010) Unphosphorylated CsgD controls biofilm formation in Salmonella enterica serovar Typhimurium. Mol Microbiol 77(3):771–786. https://doi.org/10.1111/j.1365-2958.2010.07247.x

    Article  CAS  PubMed  Google Scholar 

  71. Weber H, Pesavento C, Possling A, Tischendorf G, Hengge R (2006) Cyclic-di-GMP-mediated signalling within the sigma network of Escherichia coli. Mol Microbiol 62(4):1014–1034. https://doi.org/10.1111/j.1365-2958.2006.05440.x

    Article  CAS  PubMed  Google Scholar 

  72. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  73. 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

    Article  CAS  PubMed  Google Scholar 

  74. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  75. Wang YC, Chin KH, Tu ZL, He J, Jones CJ, Sanchez DZ, Yildiz FH, Galperin MY, Chou SH (2016) Nucleotide binding by the widespread high-affinity cyclic di-GMP receptor MshEN domain. Nat Commun 7:12481. https://doi.org/10.1038/ncomms12481

  76. Roelofs KG, Jones CJ, Helman SR, Shang X, Orr MW, Goodson JR, Galperin MY, Yildiz FH, Lee VT (2015) Systematic identification of cyclic-di-GMP binding proteins in Vibrio cholerae reveals a novel class of cyclic-di-GMP-binding ATPases associated with Type II secretion systems. PLOS Pathog 11 (10):e1005232

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  77. Jones CJ, Utada A, Davis KR, Thongsomboon W, Sanchez DZ, Banakar V, Cegelski L, Wong GCL, Yildiz FH, Parsek MR (2015) C-di-GMP regulates motile to sessile transition by modulating MshA pili biogenesis and near-surface motility behavior in Vibrio cholerae. PLOS Pathog 11 (10):e1005068

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  78. Wang Y, Kim KS (2000) Effect of rpoS mutations on stress-resistance and invasion of brain microvascular endothelial cells in Escherichia coli K1. FEMS Microbiol Lett 182(2):241–247

    Article  CAS  PubMed  Google Scholar 

  79. Schellhorn HE, Hassan HM (1988) Transcriptional regulation of katE in Escherichia coli K-12. J Bacteriol 170(9):4286–4292

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  80. Lange R, Hengge-Aronis R (1991) Identification of a central regulator of stationary-phase gene expression in Escherichia coli. Mol Microbiol 5(1):49–59. https://doi.org/10.1111/j.1365-2958.1991.tb01825.x

    Article  CAS  PubMed  Google Scholar 

  81. Battesti A, Majdalani N, Gottesman S (2011) The RpoS-mediated general stress response in Escherichia coli. Annu Rev Microbiol 65:189–213. https://doi.org/10.1146/annurev-micro-090110-102946

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  82. Hengge-Aronis R (2002) Signal transduction and regulatory mechanisms involved in control of the sigma(S) (RpoS) subunit of RNA polymerase. Microbiol Mol Biol Rev 66(3):373–395

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  83. Adams JL, McLean RJ (1999) Impact of rpoS deletion on Escherichia coli biofilms. Appl Environ Microbiol 65(9):4285–4287

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  84. Moriel DG, Bertoldi I, Spagnuolo A, Marchi S, Rosini R, Nesta B, Pastorello I, Corea VA, Torricelli G, Cartocci E, Savino S, Scarselli M, Dobrindt U, Hacker J, Tettelin H, Tallon LJ, Sullivan S, Wieler LH, Ewers C, Pickard D, Dougan G, Fontana MR, Rappuoli R, Pizza M, Serino L (2010) Identification of protective and broadly conserved vaccine antigens from the genome of extraintestinal pathogenic Escherichia coli. Proc Natl Acad Sci U S A 107(20):9072–9077. https://doi.org/10.1073/pnas.0915077107

    Article  PubMed  PubMed Central  Google Scholar 

  85. Silver RP, Aaronson W, Sutton A, Schneerson R (1980) Comparative analysis of plasmids and some metabolic characteristics of Escherichia coli K1 from diseased and healthy individuals. Infect Immun 29(1):200–206

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  86. Sjöström AE, Sondén B, Müller C, Rydström A, Dobrindt U, Wai SN, Uhlin BE (2009) Analysis of the sfaX(II) locus in the Escherichia coli meningitis isolate IHE3034 reveals two novel regulatory genes within the promoter-distal region of the main S fimbrial operon. Microb Pathog 46(3):150–158. https://doi.org/10.1016/j.micpath.2008.12.001

    Article  CAS  PubMed  Google Scholar 

  87. Spurbeck RR, Tarrien RJ, Mobley HL (2012) Enzymatically active and inactive phosphodiesterases and diguanylate cyclases are involved in regulation of motility or sessility in Escherichia coli CFT073. MBio 3(5):e00307-12. https://doi.org/10.1128/mBio.00307-12

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  88. Reinders A, Hee CS, Ozaki S, Mazur A, Boehm A, Schirmer T, Jenal U (2015) 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

    Article  PubMed  CAS  Google Scholar 

  89. 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):e01639-17. https://doi.org/10.1128/mBio.01639-17

    Article  PubMed  PubMed Central  Google Scholar 

  90. Cimdins A, Simm R, Li F, Luthje P, Thorell K, Sjoling A, Brauner A, Romling U (2017) Alterations of c-di-GMP turnover proteins modulate semi-constitutive rdar biofilm formation in commensal and uropathogenic Escherichia coli. Microbiology 6(5):e00508. https://doi.org/10.1002/mbo3.508

    Article  CAS  Google Scholar 

  91. Korhonen TK, Valtonen MV, Parkkinen J, Vaisanen-Rhen V, Finne J, Orskov F, Orskov I, Svenson SB, Makela PH (1985) Serotypes, hemolysin production, and receptor recognition of Escherichia coli strains associated with neonatal sepsis and meningitis. Infect Immun 48(2):486–491

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  92. Pesavento C, Becker G, Sommerfeldt N, Possling A, Tschowri N, Mehlis A, Hengge R (2008) Inverse regulatory coordination of motility and curli-mediated adhesion in Escherichia coli. Genes Dev 22(17):2434–2446. https://doi.org/10.1101/gad.475808

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  93. 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

    Article  CAS  PubMed  Google Scholar 

  94. Boehm A, Steiner S, Zaehringer F, Casanova A, Hamburger F, Ritz D, Keck W, Ackermann M, Schirmer T, Jenal U (2009) Second messenger signalling governs Escherichia coli biofilm induction upon ribosomal stress. Mol Microbiol 72(6):1500–1516. https://doi.org/10.1111/j.1365-2958.2009.06739.x

    Article  CAS  PubMed  Google Scholar 

  95. Romeo T (2008) Bacterial biofilms. Current topics in microbiology and immunology, vol 322. Springer, Berlin

    Google Scholar 

  96. Rossi E, Cimdins A, Luthje P, Brauner A, Sjoling A, Landini P, Romling U (2018) “It’s a gut feeling” – Escherichia coli biofilm formation in the gastrointestinal tract environment. Crit Rev Microbiol 44(1):1–30. https://doi.org/10.1080/1040841X.2017.1303660

    Article  CAS  PubMed  Google Scholar 

  97. 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

    Article  CAS  PubMed  Google Scholar 

  98. Olsen A, Jonsson A, Normark S (1989) Fibronectin binding mediated by a novel class of surface organelles on Escherichia coli. Nature 338(6217):652–655. https://doi.org/10.1038/338652a0

    Article  CAS  PubMed  Google Scholar 

  99. Bian Z, Normark S (1997) Nucleator function of CsgB for the assembly of adhesive surface organelles in Escherichia coli. EMBO J 16(19):5827–5836. https://doi.org/10.1093/emboj/16.19.5827

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  100. Römling U (2002) Molecular biology of cellulose production in bacteria. Res Microbiol 153(4):205–212

    Article  PubMed  Google Scholar 

  101. Romling U, Rohde M, Olsen A, Normark S, Reinkoster J (2000) AgfD, the checkpoint of multicellular and aggregative behaviour in Salmonella typhimurium regulates at least two independent pathways. Mol Microbiol 36(1):10–23

    Article  CAS  PubMed  Google Scholar 

  102. Morgan JL, McNamara JT, Zimmer J (2014) Mechanism of activation of bacterial cellulose synthase by cyclic di-GMP. Nat Struct Mol Biol 21(5):489–496. https://doi.org/10.1038/nsmb.2803

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  103. Vidal O, Longin R, Prigent-Combaret C, Dorel C, Hooreman M, Lejeune P (1998) Isolation of an Escherichia coli K-12 mutant strain able to form biofilms on inert surfaces: involvement of a new ompR allele that increases curli expression. J Bacteriol 180(9):2442–2449

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  104. Ferrieres L, Clarke DJ (2003) The RcsC sensor kinase is required for normal biofilm formation in Escherichia coli K-12 and controls the expression of a regulon in response to growth on a solid surface. Mol Microbiol 50(5):1665–1682

    Article  CAS  PubMed  Google Scholar 

  105. Barnhart MM, Chapman MR (2006) Curli biogenesis and function. Annu Rev Microbiol 60:131–147. https://doi.org/10.1146/annurev.micro.60.080805.142106

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  106. Bian Z, Brauner A, Li Y, Normark S (2000) Expression of and cytokine activation by Escherichia coli curli fibers in human sepsis. J Infect Dis 181(2):602–612. https://doi.org/10.1086/315233

    Article  CAS  PubMed  Google Scholar 

  107. Bokranz W, Wang X, Tschape H, Romling U (2005) Expression of cellulose and curli fimbriae by Escherichia coli isolated from the gastrointestinal tract. J Med Microbiol 54(Pt 12):1171–1182. https://doi.org/10.1099/jmm.0.46064-0

    Article  CAS  PubMed  Google Scholar 

  108. Monteiro C, Saxena I, Wang X, Kader A, Bokranz W, Simm R, Nobles D, Chromek M, Brauner A, Brown RM, Römling U (2009) Characterization of cellulose production in Escherichia coli Nissle 1917 and its biological consequences. Environ Microbiol 11(5):1105–1116. https://doi.org/10.1111/j.1462-2920.2008.01840.x

    Article  CAS  PubMed  Google Scholar 

  109. Hammar M, Arnqvist A, Bian Z, Olsen A, Normark S (1995) Expression of two csg operons is required for production of fibronectin- and Congo red-binding curli polymers in Escherichia coli K-12. Mol Microbiol 18(4):661–670

    Article  CAS  PubMed  Google Scholar 

  110. Kai-Larsen Y, Lüthje P, Chromek M, Peters V, Wang X, Holm A, Kádas 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  111. Carter MQ, Parker CT, Louie JW, Huynh S, Fagerquist CK, Mandrell RE (2012) RcsB contributes to the distinct stress fitness among Escherichia coli O157:H7 curli variants of the 1993 hamburger-associated outbreak strains. Appl Environ Microbiol 78(21):7706–7719. https://doi.org/10.1128/AEM.02157-12

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  112. Hufnagel DA, DePas WH, Chapman MR (2014) The disulfide bonding system suppresses CsgD-independent cellulose production in Escherichia coli. J Bacteriol 196(21):3690–3699. https://doi.org/10.1128/JB.02019-14

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  113. Da Re S, Ghigo JM (2006) A CsgD-independent pathway for cellulose production and biofilm formation in Escherichia coli. J Bacteriol 188(8):3073–3087. https://doi.org/10.1128/JB.188.8.3073-3087.2006

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  114. Uhlich GA, Keen JE, Elder RO (2001) Mutations in the csgD promoter associated with variations in curli expression in certain strains of Escherichia coli O157:H7. Appl Environ Microbiol 67(5):2367–2370. https://doi.org/10.1128/AEM.67.5.2367-2370.2001

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  115. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  116. Busch A, Waksman G (2012) Chaperone-usher pathways: diversity and pilus assembly mechanism. Philos Trans R Soc Lond Ser B Biol Sci 367(1592):1112–1122. https://doi.org/10.1098/rstb.2011.0206

    Article  CAS  Google Scholar 

  117. Buchanan K, Falkow S, Hull RA, Hull SI (1985) Frequency among Enterobacteriaceae of the DNA sequences encoding type 1 pili. J Bacteriol 162(2):799–803

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  118. Connell I, Agace W, Klemm P, Schembri M, Mărild S, Svanborg C (1996) Type 1 fimbrial expression enhances Escherichia coli virulence for the urinary tract. Proc Natl Acad Sci U S A 93(18):9827–9832

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  119. Müller CM, Aberg A, Straseviçiene J, Emody L, Uhlin BE, Balsalobre C (2009) Type 1 fimbriae, a colonization factor of uropathogenic Escherichia coli, are controlled by the metabolic sensor CRP-cAMP. PLoS Pathog 5(2):e1000303. https://doi.org/10.1371/journal.ppat.1000303

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  120. Martinez JJ, Mulvey MA, Schilling JD, Pinkner JS, Hultgren SJ (2000) Type 1 pilus-mediated bacterial invasion of bladder epithelial cells. EMBO J 19(12):2803–2812. https://doi.org/10.1093/emboj/19.12.2803

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  121. Martinez JJ, Hultgren SJ (2002) Requirement of rho-family GTPases in the invasion of type 1-piliated uropathogenic Escherichia coli. Cell Microbiol 4(1):19–28

    Article  CAS  PubMed  Google Scholar 

  122. Gunther NW, Snyder JA, Lockatell V, Blomfield I, Johnson DE, Mobley HL (2002) Assessment of virulence of uropathogenic Escherichia coli type 1 fimbrial mutants in which the invertible element is phase-locked on or off. Infect Immun 70(7):3344–3354

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  123. Teng CH, Cai M, Shin S, Xie Y, Kim KJ, Khan NA, Di Cello F, Kim KS (2005) Escherichia coli K1 RS218 interacts with human brain microvascular endothelial cells via type 1 fimbria bacteria in the fimbriated state. Infect Immun 73(5):2923–2931. https://doi.org/10.1128/IAI.73.5.2923-2931.2005

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  124. Saukkonen KM, Nowicki B, Leinonen M (1988) Role of type 1 and S fimbriae in the pathogenesis of Escherichia coli O18:K1 bacteremia and meningitis in the infant rat. Infect Immun 56(4):892–897

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  125. Zhou G, Mo WJ, Sebbel P, Min G, Neubert TA, Glockshuber R, Wu XR, Sun TT, Kong XP (2001) Uroplakin Ia is the urothelial receptor for uropathogenic Escherichia coli: evidence from in vitro FimH binding. J Cell Sci 114(Pt 22):4095–4103

    CAS  PubMed  Google Scholar 

  126. Brinton CC Jr (1959) Non-flagellar appendages of bacteria. Nature 183(4664):782–786

    Article  PubMed  Google Scholar 

  127. Spurbeck RR, Stapleton AE, Johnson JR, Walk ST, Hooton TM, Mobley HL (2011) Fimbrial profiles predict virulence of uropathogenic Escherichia coli strains: contribution of Ygi and Yad fimbriae. Infect Immun 79(12):4753–4763. https://doi.org/10.1128/IAI.05621-11

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  128. Marklund BI, Tennent JM, Garcia E, Hamers A, Baga M, Lindberg F, Gaastra W, Normark S (1992) Horizontal gene transfer of the Escherichia coli pap and prs pili operons as a mechanism for the development of tissue-specific adhesive properties. Mol Microbiol 6(16):2225–2242

    Article  CAS  PubMed  Google Scholar 

  129. Hull RA, Gill RE, Hsu P, Minshew BH, Falkow S (1981) Construction and expression of recombinant plasmids encoding type 1 or D-mannose-resistant pili from a urinary tract infection Escherichia coli isolate. Infect Immun 33(3):933–938

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  130. Virkola R, Westerlund B, Holthofer H, Parkkinen J, Kekomaki M, Korhonen TK (1988) Binding characteristics of Escherichia coli adhesins in human urinary bladder. Infect Immun 56(10):2615–2622

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  131. Stins MF, Prasadarao NV, Ibric L, Wass CA, Luckett P, Kim KS (1994) Binding characteristics of S fimbriated Escherichia coli to isolated brain microvascular endothelial cells. Am J Pathol 145(5):1228–1236

    CAS  PubMed  PubMed Central  Google Scholar 

  132. Korhonen TK, Parkkinen J, Hacker J, Finne J, Pere A, Rhen M, Holthofer H (1986) Binding of Escherichia coli S fimbriae to human kidney epithelium. Infect Immun 54(2):322–327

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  133. Parkkinen J, Korhonen TK, Pere A, Hacker J, Soinila S (1988) Binding sites in the rat brain for Escherichia coli S fimbriae associated with neonatal meningitis. J Clin Invest 81(3):860–865. https://doi.org/10.1172/JCI113395

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  134. Parkkinen J, Ristimaki A, Westerlund B (1989) Binding of Escherichia coli S fimbriae to cultured human endothelial cells. Infect Immun 57(7):2256–2259

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  135. Prasadarao NV, Wass CA, Hacker J, Jann K, Kim KS (1993) Adhesion of S-fimbriated Escherichia coli to brain glycolipids mediated by sfaA gene-encoded protein of S-fimbriae. J Biol Chem 268(14):10356–10363

    CAS  PubMed  Google Scholar 

  136. Knapp S, Hacker J, Jarchau T, Goebel W (1986) Large, unstable inserts in the chromosome affect virulence properties of uropathogenic Escherichia coli O6 strain 536. J Bacteriol 168(1):22–30

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  137. Hacker J, Kaper JB (2000) Pathogenicity islands and the evolution of microbes. Annu Rev Microbiol 54:641–679. https://doi.org/10.1146/annurev.micro.54.1.641

    Article  CAS  PubMed  Google Scholar 

  138. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  139. 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

    Article  PubMed  PubMed Central  Google Scholar 

  140. Ferenci T (2005) Maintaining a healthy SPANC balance through regulatory and mutational adaptation. Mol Microbiol 57(1):1–8. https://doi.org/10.1111/j.1365-2958.2005.04649.x

    Article  CAS  PubMed  Google Scholar 

  141. Uhlich GA, Chen CY, Cottrell BJ, Hofmann CS, Dudley EG, Strobaugh TP, Nguyen LH (2013) Phage insertion in mlrA and variations in rpoS limit curli expression and biofilm formation in Escherichia coli serotype O157: H7. Microbiology 159(Pt 8):1586–1596. https://doi.org/10.1099/mic.0.066118-0

    Article  CAS  PubMed  Google Scholar 

  142. Lutgens M, Gottschalk G (1980) Why a co-substrate is required for anaerobic growth of Escherichia coli on citrate. J Gen Microbiol 119(1):63–70. https://doi.org/10.1099/00221287-119-1-63

    Article  CAS  PubMed  Google Scholar 

  143. Lara FJ, Stokes JL (1952) Oxidation of citrate by Escherichia coli. J Bacteriol 63(3):415–420

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  144. Ishiguro N, Oka C, Sato G (1978) Isolation of citrate-positive variants of Escherichia coli from domestic pigeons, pigs, cattle and horses. Appl Environ Microbiol 36(2):217–222

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  145. Ishiguro N, Oka C, Hanzawa Y, Sato G (1979) Plasmids in Escherichia coli controlling citrate-utilizing ability. Appl Environ Microbiol 38(5):956–964

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  146. Blount ZD, Barrick JE, Davidson CJ, Lenski RE (2012) Genomic analysis of a key innovation in an experimental Escherichia coli population. Nature 489(7417):513–518. https://doi.org/10.1038/nature11514

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  147. Smith HW, Parsell Z, Green P (1978) Thermosensitive H1 plasmids determining citrate utilization. J Gen Microbiol 109(2):305–311. https://doi.org/10.1099/00221287-109-2-305

    Article  CAS  PubMed  Google Scholar 

  148. Notley-McRobb L, King T, Ferenci T (2002) rpoS mutations and loss of general stress resistance in Escherichia coli populations as a consequence of conflict between competing stress responses. J Bacteriol 184(3):806–811

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  149. Simmons J (1926) A culture medium for differentiating organisms of typhoid-colon Aerogenes groups and for isolation of certain fungi: with colored plate. J Infect Dis 39(Issue 3):209–214

    Article  Google Scholar 

  150. Koser SA (1924) Correlation of citrate utilization by members of the colon-Aerogenes group with other differential characteristics and with habitat. J Bacteriol 9(1):59–77

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  151. Carter MQ, Louie JW, Huynh S, Parker CT (2014) Natural rpoS mutations contribute to population heterogeneity in Escherichia coli O157:H7 strains linked to the 2006 US spinach-associated outbreak. Food Microbiol 44:108–118. https://doi.org/10.1016/j.fm.2014.05.021

    Article  CAS  PubMed  Google Scholar 

  152. Carter MQ, Brandl MT, Louie JW, Kyle JL, Carychao DK, Cooley MB, Parker CT, Bates AH, Mandrell RE (2011) Distinct acid resistance and survival fitness displayed by Curli variants of enterohemorrhagic Escherichia coli O157:H7. Appl Environ Microbiol 77(11):3685–3695. https://doi.org/10.1128/AEM.02315-10

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  153. Kurtz I (2014) Molecular mechanisms and regulation of urinary acidification. Compr Physiol 4(4):1737–1774. https://doi.org/10.1002/cphy.c140021

    Article  PubMed  PubMed Central  Google Scholar 

  154. Plough IC, Baker EM (1959) Maximum physiological concentration of sodium in human urine. J Appl Physiol 14:1036–1038. https://doi.org/10.1152/jappl.1959.14.6.1036

    Article  CAS  PubMed  Google Scholar 

  155. Giannakopoulos X, Evangelou A, Kalfakakou V, Grammeniatis E, Papandropoulos I, Charalambopoulos K (1997) Human bladder urine oxygen content: implications for urinary tract diseases. Int Urol Nephrol 29(4):393–401

    Article  CAS  PubMed  Google Scholar 

  156. Gupta RC, Goyal A, Ghosh R, Punjabi M, Singh PP (1982) Normal range for glucose in urine: age-related changes. Clin Chem 28(11):2335

    Article  CAS  PubMed  Google Scholar 

  157. Jain S (1986) Reference interval for urinary glucose in elderly subjects. Clin Chem 32(4):711–712

    Article  CAS  PubMed  Google Scholar 

  158. Edin-Liljegren A, Rodin L, Grenabo L, Hedelin H (2001) The importance of glucose for the Escherichia coli mediated citrate depletion in synthetic and human urine. Scand J Urol Nephrol 35(2):106–111

    CAS  PubMed  Google Scholar 

  159. Brooks T, Keevil CW (1997) A simple artificial urine for the growth of urinary pathogens. Lett Appl Microbiol 24(3):203–206

    Article  CAS  PubMed  Google Scholar 

  160. Alteri CJ, Smith SN, Mobley HL (2009) Fitness of Escherichia coli during urinary tract infection requires gluconeogenesis and the TCA cycle. PLoS Pathog 5(5):e1000448. https://doi.org/10.1371/journal.ppat.1000448

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  161. Anfora AT, Haugen BJ, Roesch P, Redford P, Welch RA (2007) Roles of serine accumulation and catabolism in the colonization of the murine urinary tract by Escherichia coli CFT073. Infect Immun 75(11):5298–5304. https://doi.org/10.1128/IAI.00652-07

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  162. Snyder JA, Haugen BJ, Buckles EL, Lockatell CV, Johnson DE, Donnenberg MS, Welch RA, Mobley HL (2004) Transcriptome of uropathogenic Escherichia coli during urinary tract infection. Infect Immun 72(11):6373–6381. https://doi.org/10.1128/IAI.72.11.6373-6381.2004

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  163. Conover MS, Hadjifrangiskou M, Palermo JJ, Hibbing ME, Dodson KW, Hultgren SJ (2016) Metabolic requirements of Escherichia coli in intracellular bacterial communities during urinary tract infection pathogenesis. MBio 7(2):e00104–e00116. https://doi.org/10.1128/mBio.00104-16

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  164. Galperin MY, Nikolskaya AN, Koonin EV (2001) Novel domains of the prokaryotic two-component signal transduction systems. FEMS Microbiol Lett 203(1):11–21. https://doi.org/10.1111/j.1574-6968.2001.tb10814.x

    Article  CAS  PubMed  Google Scholar 

  165. Crichton RR (2009) Iron metabolism: from molecular mechanisms to clinical consequences, 3rd edn. Wiley, Chichester

    Book  Google Scholar 

  166. Winterbourn CC (1995) Toxicity of iron and hydrogen peroxide: the Fenton reaction. Toxicol Lett 82–83:969–974

    Article  PubMed  Google Scholar 

  167. DePas WH, Hufnagel DA, Lee JS, Blanco LP, Bernstein HC, Fisher ST, James GA, Stewart PS, Chapman MR (2013) Iron induces bimodal population development by Escherichia coli. Proc Natl Acad Sci U S A 110(7):2629–2634. https://doi.org/10.1073/pnas.1218703110

    Article  PubMed  PubMed Central  Google Scholar 

  168. Smith JL (2004) The physiological role of ferritin-like compounds in bacteria. Crit Rev Microbiol 30(3):173–185. https://doi.org/10.1080/10408410490435151

    Article  CAS  PubMed  Google Scholar 

  169. Grass G, Otto M, Fricke B, Haney CJ, Rensing C, Nies DH, Munkelt D (2005) FieF (YiiP) from Escherichia coli mediates decreased cellular accumulation of iron and relieves iron stress. Arch Microbiol 183(1):9–18. https://doi.org/10.1007/s00203-004-0739-4

    Article  CAS  PubMed  Google Scholar 

  170. Crosa JH (1984) The relationship of plasmid-mediated iron transport and bacterial virulence. Annu Rev Microbiol 38:69–89. https://doi.org/10.1146/annurev.mi.38.100184.000441

    Article  CAS  PubMed  Google Scholar 

  171. Garénaux A, Caza M, Dozois CM (2011) The ins and outs of siderophore mediated iron uptake by extra-intestinal pathogenic Escherichia coli. Vet Microbiol 153(1–2):89–98. https://doi.org/10.1016/j.vetmic.2011.05.023

    Article  CAS  PubMed  Google Scholar 

  172. Johnson JR (1991) Virulence factors in Escherichia coli urinary tract infection. Clin Microbiol Rev 4(1):80–128

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  173. Sik Kim K (2006) Meningitis-associated Escherichia coli. EcoSal Plus 2(1). https://doi.org/10.1128/ecosalplus.8.6.1.2

  174. Montgomerie JZ, Bindereif A, Neilands JB, Kalmanson GM, Guze LB (1984) Association of hydroxamate siderophore (aerobactin) with Escherichia coli isolated from patients with bacteremia. Infect Immun 46(3):835–838

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  175. Kortman GA, Raffatellu M, Swinkels DW, Tjalsma H (2014) Nutritional iron turned inside out: intestinal stress from a gut microbial perspective. FEMS Microbiol Rev 38(6):1202–1234. https://doi.org/10.1111/1574-6976.12086

    Article  CAS  PubMed  Google Scholar 

  176. Cartron ML, Maddocks S, Gillingham P, Craven CJ, Andrews SC (2006) Feo--transport of ferrous iron into bacteria. Biometals 19(2):143–157. https://doi.org/10.1007/s10534-006-0003-2

    Article  CAS  PubMed  Google Scholar 

  177. Grosse C, Scherer J, Koch D, Otto M, Taudte N, Grass G (2006) A new ferrous iron-uptake transporter, EfeU (YcdN) from Escherichia coli. Mol Microbiol 62(1):120–131. https://doi.org/10.1111/j.1365-2958.2006.05326.x

    Article  CAS  PubMed  Google Scholar 

  178. Wagegg W, Braun V (1981) Ferric citrate transport in Escherichia coli requires outer membrane receptor protein fecA. J Bacteriol 145(1):156–163

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  179. Banerjee S, Paul S, Nguyen LT, Chu BC, Vogel HJ (2016) FecB, a periplasmic ferric-citrate transporter from E. coli, can bind different forms of ferric-citrate as well as a wide variety of metal-free and metal-loaded tricarboxylic acids. Metallomics 8(1):125–133. https://doi.org/10.1039/c5mt00218d

    Article  CAS  PubMed  Google Scholar 

  180. Enz S, Brand H, Orellana C, Mahren S, Braun V (2003) Sites of interaction between the FecA and FecR signal transduction proteins of ferric citrate transport in Escherichia coli K-12. J Bacteriol 185(13):3745–3752

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  181. Hussein S, Hantke K, Braun V (1981) Citrate-dependent iron transport system in Escherichia coli K-12. Eur J Biochem 117(2):431–437

    Article  CAS  PubMed  Google Scholar 

  182. Pos KM, Dimroth P, Bott M (1998) The Escherichia coli citrate carrier CitT: a member of a novel eubacterial transporter family related to the 2-oxoglutarate/malate translocator from spinach chloroplasts. J Bacteriol 180(16):4160–4165

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  183. Iida-Tanaka K, Tanaka T, Irino S, Nagayama A (1986) Enhanced bactericidal action of mouse macrophages by subinhibitory concentrations of monobactams. J Antimicrob Chemother 18(2):239–250

    Article  CAS  PubMed  Google Scholar 

  184. Hall BG (1997) The rtn gene of Proteus vulgaris is actually from Escherichia coli. J Bacteriol 179(7):2433–2434. https://doi.org/10.1128/jb.179.7.2433-2434.1997

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgments

We are grateful to Prof. Dr. Ulrich Dobrindt for valuable comments on this work. Research in the authors’ laboratory is supported by grants from the Swedish Research Council (2015-03007, 2015-06824, 2016-06598, 349-2007-8673, and 829-2006-7431).

Author information

Authors and Affiliations

  1. Department of Molecular Biology, The Laboratory for Molecular Infection Medicine Sweden (MIMS), Umeå Centre for Microbial Research (UCMR), Umeå University, Umeå, Sweden

    Nikola Zlatkov & Bernt Eric Uhlin

Authors
  1. Nikola Zlatkov
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Bernt Eric Uhlin
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Bernt Eric Uhlin .

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

Zlatkov, N., Uhlin, B.E. (2020). Unconventional Cyclic di-GMP Signaling in Escherichia coli . 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_29

Download citation

Publish with us

Policies and ethics

Search

Navigation