1887

Abstract

Switching from the motile planktonic bacterial lifestyle to a biofilm existence is stimulated by the signalling molecule bis-(3′-5′)-cyclic-diguanosine monophosphate (cyclic-di-GMP), which is antagonistically controlled by diguanylate cyclases (DGCs; characterized by GGDEF domains) and specific phosphodiesterases (PDEs; mostly featuring EAL domains). Here, we present the expression patterns of all 28 genes that encode GGDEF/EAL domain proteins in K-12. Twenty-one genes are expressed in Luria–Bertani medium, with 15 being under control. While a small subset of GGDEF/EAL proteins (YeaJ and YhjH) is dominant and modulates motility in post-exponentially growing cells, a diverse battery of GGDEF/EAL proteins is deployed during entry into stationary phase, especially in cells grown at reduced temperature (28 °C). This suggests that multiple signal input into cyclic-di-GMP control is particularly important in growth-restricted cells in an extra-host environment. Six GGDEF/EAL genes differentially control the expression of adhesive curli fimbriae. Besides the previously described , , and genes, these are (), which stimulates the expression of the DGC YdaM and the major curli regulator CsgD, and , which contributes to expression of the curli structural operon . Finally, we discuss why other GGDEF/EAL domain-encoding genes, despite being expressed, do not influence motility and/or curli formation.

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2009-04-01
2019-10-18
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References

  1. Adler, J. & Templeton, B. ( 1967; ). The effect of environmental conditions on the motility of Escherichia coli. J Gen Microbiol 46, 175–184.[CrossRef]
    [Google Scholar]
  2. Amikam, D. & Galperin, M. Y. ( 2006; ). PilZ domain is part of the bacterial c-di-GMP binding protein. Bioinformatics 22, 3–6.[CrossRef]
    [Google Scholar]
  3. Amsler, C. D., Cho, M. & Matsumura, P. ( 1993; ). Multiple factors underlying the maximum motility of Escherichia coli as cultures enter post-exponential growth. J Bacteriol 175, 6238–6244.
    [Google Scholar]
  4. Beloin, C., Roux, A. & Ghigo, J.-M. ( 2008; ). Escherichia coli biofilms. Curr Top Microbiol Immunol 322, 249–289.
    [Google Scholar]
  5. Benach, J., Swaminathan, S. S., Tamayo, R., Handelman, S. K., Folta-Stogniew, E., Ramos, J. E., Forouhar, F., Neely, H., Seetharaman, J. & other authors ( 2007; ). The structural basis of cyclic diguanylate signal transduction by PilZ domains. EMBO J 26, 5153–5166.[CrossRef]
    [Google Scholar]
  6. Brombacher, E., Baratto, A., Dorel, C. & Landini, P. ( 2006; ). Gene expression regulation by the curli activator CsgD protein: modulation of cellulose biosynthesis and control of negative determinants for microbial adhesion. J Bacteriol 188, 2027–2037.[CrossRef]
    [Google Scholar]
  7. Brown, P. K., Dozois, C. M., Nickerson, C. A., Zuppardo, A., Terlonge, J. & Curtiss, R., III ( 2001; ). MlrA, a novel regulator of curli (Agf) and extracellular matrix synthesis by Escherichia coli and Salmonella enterica serovar Typhimurium. Mol Microbiol 41, 349–363.[CrossRef]
    [Google Scholar]
  8. Chang, A. L., Tuckerman, J. R., Gonzalez, G., Mayer, R., Weinhouse, H., Volman, G., Amikam, D., Benziman, M. & Gilles-Gonzalez, M.-A. ( 2001; ). Phosphodiesterase A1, a regulator of cellulose synthesis in Acetobacter xylinum, is a heme-based sensor. Biochemistry 40, 3420–3426.[CrossRef]
    [Google Scholar]
  9. Christen, M., Christen, B., Folcher, M., Schauerte, A. & Jenal, U. ( 2005; ). Identification and characterization of a cyclic di-GMP-specific phosphodiesterase and its allosteric control by GTP. J Biol Chem 280, 30829–30837.[CrossRef]
    [Google Scholar]
  10. Christen, M., Christen, B., Allan, M. G., Folcher, M., Jenö, P., Grzesiek, S. & Jenal, U. ( 2007; ). DgrA is a member of a new family of cyclic diguanosine monophosphate receptors and controls flagellar motor function in Caulobacter crescentus. Proc Natl Acad Sci U S A 104, 4112–4117.[CrossRef]
    [Google Scholar]
  11. Datsenko, K. A. & Wanner, B. L. ( 2000; ). One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc Natl Acad Sci U S A 97, 6640–6645.[CrossRef]
    [Google Scholar]
  12. Frye, J., Karlinsey, J. E., Felise, H. R., Marzolf, B., Dowidar, N., McClelland, M. & Hughes, K. T. ( 2006; ). Identification of new flagellar genes of Salmonella enterica serovar Typhimurium. J Bacteriol 188, 2233–2243.[CrossRef]
    [Google Scholar]
  13. Gerstel, U., Park, C. & Römling, U. ( 2003; ). Complex regulation of csgD promoter activity by global regulatory proteins. Mol Microbiol 49, 639–654.
    [Google Scholar]
  14. Girgis, H. S., Liu, Y., Ryu, W. S. & Tavazoie, S. ( 2007; ). A comprehensive genetic characterization of bacterial motility. PLoS Genet 3, e154 [CrossRef]
    [Google Scholar]
  15. Gruber, T. M. & Gross, C. A. ( 2003; ). Multiple sigma subunits and the partitioning of bacterial transcription space. Annu Rev Microbiol 57, 441–466.[CrossRef]
    [Google Scholar]
  16. Hayashi, K., Morooka, N., Yamamoto, Y., Fujita, K., Isono, K., Choi, S., Ohtsubo, E., Baba, T., Wanner, B. L. & other authors ( 2006; ). Highly accurate genome sequences of Escherichia coli K-12 strains MG1655 and W3110. Mol Syst Biol 2, 2006.0007
    [Google Scholar]
  17. Hickman, J. W. & Harwood, C. S. ( 2008; ). Identification of FleQ from Pseudomonas aeruginosa as a c-di-GMP-responsive transcription factor. Mol Microbiol 69, 376–389.[CrossRef]
    [Google Scholar]
  18. Hickman, J. W., Tifrea, D. F. & Harwood, C. S. ( 2005; ). A chemosensory system that regulates biofilm formation through modulation of cyclic diguanylate levels. Proc Natl Acad Sci U S A 102, 14422–14427.[CrossRef]
    [Google Scholar]
  19. Jenal, U. & Malone, J. ( 2006; ). Mechanisms of cyclic-di-GMP signaling in bacteria. Annu Rev Genet 40, 385–407.[CrossRef]
    [Google Scholar]
  20. Jonas, K., Edwards, A. N., Simm, R., Romeo, T., Römling, U. & Melefors, O. ( 2008; ). The RNA binding protein CsrA controls c-di-GMP metabolism by directly regulating the expression of GGDEF proteins. Mol Microbiol 70, 236–257.[CrossRef]
    [Google Scholar]
  21. 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, 602–616.[CrossRef]
    [Google Scholar]
  22. 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, 371–382.[CrossRef]
    [Google Scholar]
  23. Kulasakara, H., Lee, E., Brencic, A., Liberati, N., Urbach, J., Miyata, S., Lee, D. G., Neely, A. N., Hyodo, M. & other authors ( 2006; ). Analysis of Pseudomonas aeruginosa diguanylate cyclases and phosphodiesterase reveals a role for bis-(3′-5′)-cyclic-GMP in virulence. Proc Natl Acad Sci U S A 103, 2839–2844.[CrossRef]
    [Google Scholar]
  24. Lange, R. & Hengge-Aronis, R. ( 1991; ). Identification of a central regulator of stationary-phase gene expression in Escherichia coli. Mol Microbiol 5, 49–59.[CrossRef]
    [Google Scholar]
  25. Lange, R. & Hengge-Aronis, R. ( 1994; ). The cellular concentration of the σ S subunit of RNA-polymerase in Escherichia coli is controlled at the levels of transcription, translation and protein stability. Genes Dev 8, 1600–1612.[CrossRef]
    [Google Scholar]
  26. Lee, V. T., Matewish, J. M., Kessler, J. L., Hyodo, M., Hayakawa, Y. & Lory, S. ( 2007; ). A cyclic-di-GMP receptor required for bacterial exopolysaccharide production. Mol Microbiol 65, 1474–1484.[CrossRef]
    [Google Scholar]
  27. Malone, J. G., Williams, R., Christen, M., Jenal, U., Spiers, A. J. & Rainey, P. B. ( 2007; ). The structure–function relationship of WspR, a Pseudomonas fluorescens response regulator with a GGDEF output domain. Microbiology 153, 980–994.[CrossRef]
    [Google Scholar]
  28. Méndez-Ortiz, M. M., Hyodo, M., Hayakawa, Y. & Membrillo-Hernández, J. ( 2006; ). Genome wide transcription profile of Escherichia coli in response to high levels of the second messenger c-diGMP. J Biol Chem 281, 8090–8099.[CrossRef]
    [Google Scholar]
  29. Merighi, M., Lee, V. T., Hyodo, M., Hayakawa, Y. & Lory, S. ( 2007; ). The second messenger bis-(3′-5′)-cyclic-GMP and its PilZ domain-containing receptor Alg44 are required for alginate biosynthesis in Pseudomonas aeruginosa. Mol Microbiol 65, 876–895.[CrossRef]
    [Google Scholar]
  30. Miller, J. H. ( 1972; ). Experiments in Molecular Genetics. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
  31. Olsén, A., Jonsson, A. & Normark, S. ( 1989; ). Fibronectin binding mediated by a novel class of surface organelles on Escherichia coli. Nature 338, 652–655.[CrossRef]
    [Google Scholar]
  32. Paul, R., Weiser, S., Amiot, N., 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, 715–727.[CrossRef]
    [Google Scholar]
  33. 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, 2434–2446.[CrossRef]
    [Google Scholar]
  34. Powell, B. S., Court, D. L., Nakamura, Y., Rivas, M. P. & Turnbough, C. L., Jr ( 1994; ). Rapid confirmation of single copy lambda prophage integration by PCR. Nucleic Acids Res 22, 5765–5766.[CrossRef]
    [Google Scholar]
  35. Rao, F., Yang, Y., Qi, Y. & Liang, Z. X. ( 2008; ). Catalytic mechanism of c-di-GMP specific phosphodiesterase: a study of the EAL domain-containing RocR from Pseudomonas aeruginosa. J Bacteriol 190, 3622–3631.[CrossRef]
    [Google Scholar]
  36. Römling, U. ( 2005; ). Characterization of the rdar morphotype, a multicellular behaviour in Enterobacteriaceae. Cell Mol Life Sci 62, 1234–1246.[CrossRef]
    [Google Scholar]
  37. Römling, U., Bian, Z., Hammar, M., Sierralta, W. D. & Normark, S. ( 1998; ). Curli fibers are highly conserved between Salmonella typhimurium and Escherichia coli with respect to operon structure and regulation. J Bacteriol 180, 722–731.
    [Google Scholar]
  38. Römling, U., Rohde, M., Olsén, 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, 10–23.[CrossRef]
    [Google Scholar]
  39. Römling, U., Gomelsky, M. & Galperin, M. Y. ( 2005; ). C-di-GMP: the dawning of a novel bacterial signalling system. Mol Microbiol 57, 629–639.[CrossRef]
    [Google Scholar]
  40. Ryan, R. P., Fouhy, Y., Lucey, F. & Dow, J. M. ( 2006a; ). Cyclic di-GMP signaling in bacteria: recent advances and new puzzles. J Bacteriol 188, 8327–8334.[CrossRef]
    [Google Scholar]
  41. Ryan, R. P., Fouhy, Y., Lucey, J. F., Crossman, L. C., Spiro, S., He, Y.-W., Zhang, L.-H., Heeb, S., Williams, P. & Dow, J. M. ( 2006b; ). Cell–cell signaling in Xanthomonas campestris involves an HD-GYP domain protein that functions in cyclic di-GMP turnover. Proc Natl Acad Sci U S A 103, 6712–6717.[CrossRef]
    [Google Scholar]
  42. Rychlik, I., Martin, G., Methner, U., Lovell, M., Cardova, L., Sebkova, A., Sevcik, M., Damborsky, J. & Barrow, P. A. ( 2002; ). Identification of Salmonella enterica serovar Typhimurium genes associated with growth suppression in stationary-phase nutrient broth cultures and in the chicken intestine. Arch Microbiol 178, 411–420.[CrossRef]
    [Google Scholar]
  43. Ryjenkov, D. A., Tarutina, M., Moskvin, O. V. & Gomelsky, M. ( 2005; ). Cyclic diguanylate is a ubiquitous signaling molecule in bacteria: insights into biochemistry of the GGDEF protein domain. J Bacteriol 187, 1792–1798.[CrossRef]
    [Google Scholar]
  44. Ryjenkov, D. A., Simm, R., Römling, U. & Gomelsky, M. ( 2006; ). The PilZ domain is a receptor for the second messenger c-di-GMP: the PilZ protein YcgR controls motility in enterobacteria. J Biol Chem 281, 30310–30314.[CrossRef]
    [Google Scholar]
  45. Schmidt, A. J., Ryjenkov, D. A. & Gomelsky, M. ( 2005; ). The ubiquitous protein domain EAL is a cyclic diguanylate-specific phosphodiesterase: enzymatically active and inactive EAL domains. J Bacteriol 187, 4774–4781.[CrossRef]
    [Google Scholar]
  46. Simm, R., Morr, M., Kader, A., Nimtz, M. & Römling, U. ( 2004; ). GGDEF and EAL domains inversely regulate cyclic di-GMP levels and transition from sessility to motility. Mol Microbiol 53, 1123–1134.[CrossRef]
    [Google Scholar]
  47. 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, 3613–3623.[CrossRef]
    [Google Scholar]
  48. Simons, R. W., Houman, F. & Kleckner, N. ( 1987; ). Improved single and multicopy lac-based cloning vectors for protein and operon fusions. Gene 53, 85–96.[CrossRef]
    [Google Scholar]
  49. Sudarsan, N., Lee, E. R., Weinberg, Z., Moy, R. H., Kim, J. N., Link, K. H. & Breaker, R. R. ( 2008; ). Riboswitches in eubacteria sense the second messenger cyclic di-GMP. Science 321, 411–413.[CrossRef]
    [Google Scholar]
  50. Suzuki, K., Babitzke, P., Kushner, S. R. & 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, 2605–2617.[CrossRef]
    [Google Scholar]
  51. Tamayo, R., Tischler, A. D. & Camilli, A. ( 2005; ). The EAL domain protein VieA is a cyclic diguanylate phosphodiesterase. J Biol Chem 280, 33324–33330.[CrossRef]
    [Google Scholar]
  52. Tamayo, R., Pratt, J. T. & Camilli, A. ( 2007; ). Roles of cyclic diguanylate in the regulation of bacterial pathogenesis. Annu Rev Microbiol 61, 131–148.[CrossRef]
    [Google Scholar]
  53. Weber, H., Polen, T., Heuveling, J., Wendisch, V. & Hengge, R. ( 2005; ). Genome-wide analysis of the general stress response network in Escherichia coli: σ S-dependent genes, promoters and sigma factor selectivity. J Bacteriol 187, 1591–1603.[CrossRef]
    [Google Scholar]
  54. Weber, H., Pesavento, C., Possling, A., Tischendorf, G. & Hengge, R. ( 2006; ). Cyclic-di-GMP-mediated signaling within the σ S network of Escherichia coli. Mol Microbiol 62, 1014–1034.[CrossRef]
    [Google Scholar]
  55. Wolfe, A. J. & Visick, K. L. ( 2008; ). Get the message out: cyclic-di-GMP regulates multiple levels of flagellum-based motility. J Bacteriol 190, 463–475.[CrossRef]
    [Google Scholar]
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