1887

Abstract

The K-12 gene encodes a protein with domains associated with cyclic di-GMP signalling: GGDEF (associated with diguanylate cyclase activity) and EAL (associated with cyclic di-GMP phosphodiesterase activity). Here, it is shown that is expressed under anaerobic conditions from a class II FNR (regulator of fumarate and nitrate reduction)-dependent promoter. Anaerobic expression of is greatest in stationary phase, and in cultures grown at 28 °C, suggesting that low growth rates promote expression. Mutation of resulted in altered cell surface properties and enhanced sensitivity when anaerobic cultures were exposed to peroxides. The purified YfgF GGDEF-EAL (YfgF) and EAL (YfgF) domains possessed cyclic di-GMP-specific phosphodiesterase activity, but lacked diguanylate cyclase activity. However, the catalytically inactive GGDEF domain was required for YfgF dimerization and enhanced cyclic di-GMP phosphodiesterase activity in the presence of physiological concentrations of Mg. The cyclic di-GMP phosphodiesterase activity of YfgF and YfgF was inhibited by the product of the reaction, 5′-phosphoguanylyl-(3′–5′)-guanosine (pGpG). Thus, it is shown that the gene encodes an anaerobic cyclic di-GMP phosphodiesterase that is involved in remodelling the cell surface of K-12 and in the response to peroxide shock, with implications for integrating three global regulatory networks, i.e. oxygen regulation, cyclic di-GMP signalling and the oxidative stress response.

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2010-09-01
2019-10-20
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References

  1. Achebach, S., Selmer, T. & Unden, G. ( 2005; ). Properties and significance of apoFNR as a second form of air-inactivated [4Fe–4S] FNR of Escherichia coli. FEBS J 272, 4260–4269.[CrossRef]
    [Google Scholar]
  2. Anjem, A., Varghese, S. & Imlay, J. I. ( 2009; ). Manganese import is a key element of the OxyR response to hydrogen peroxide in Escherichia coli. Mol Microbiol 72, 844–858.[CrossRef]
    [Google Scholar]
  3. Antoniani, D., Bocci, P., Maciag, A., Raffaelli, N. & Landini, P. ( 2010; ). Monitoring of diguanylate cyclase activity and of cyclic-di-GMP biosynthesis by whole cell assays suitable for high-throughput screening of biofilm inhibitors. Appl Microbiol Biotechnol 85, 1095–1104.[CrossRef]
    [Google Scholar]
  4. Browning, D., Lee, D., Green, J. & Busby, S. ( 2003; ). Secrets of bacterial transcription initiation taught by the Escherichia coli FNR protein. In Signals, Switches, Regulons and Cascades: Control of Bacterial Gene Expression, pp. 127–142. Edited by Hodgson, D. A. & Thomas, C. M.. Cambridge, UK. : Cambridge University Press.
    [Google Scholar]
  5. Chan, C., Paul, R., Samoray, D., Amiot, N. C., Giese, B., Jenal, U. & Schirmer, T. ( 2004; ). Structural basis of activity and allosteric control of diguanylate cyclase. Proc Natl Acad Sci U S A 101, 17084–17089.[CrossRef]
    [Google Scholar]
  6. Chang, A. L., Tuckerman, J. R., Gonzalez, G., Mayer, R., Weinhouse, H., Volman, G., Amikan, 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]
  7. 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]
  8. 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, 32015–32024.[CrossRef]
    [Google Scholar]
  9. Claros, M. G. & von Heijne, G. ( 1994; ). TopPred II: an improved software for membrane protein structure predictions. Comput Appl Biosci 10, 685–686.
    [Google Scholar]
  10. Constantinidou, C., Hobman, J. L., Griffiths, L., Patel, M. D., Penn, C. W., Cole, J. A. & Overton, T. W. ( 2006; ). A reassessment of the FNR regulon and transcriptomic analysis of the effects of nitrate, nitrite, NarXL and NarPQ as Escherichia coli adapts from aerobic to anaerobic growth. J Biol Chem 281, 4802–4815.[CrossRef]
    [Google Scholar]
  11. Delgado-Nixon, V. M., Gonzalez, G. & Gilles-Gonzalez, M. A. ( 2000; ). Dos, a heme-binding PAS domain protein from Escherichia coli, is a direct oxygen sensor. Biochemistry 39, 2685–2691.[CrossRef]
    [Google Scholar]
  12. 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, 93–104.[CrossRef]
    [Google Scholar]
  13. Eiglmeier, K., Honore, N., Iuchi, S., Lin, E. C. C. & Cole, S. T. ( 1989; ). Molecular genetic analysis of FNR-dependent promoters. Mol Microbiol 3, 869–878.[CrossRef]
    [Google Scholar]
  14. Galperin, M. Y., Nikolskaya, A. N. & Koonin, E. V. ( 2001; ). Novel domains of the prokaryotic two-component signal transduction systems. FEMS Microbiol Lett 203, 11–21.[CrossRef]
    [Google Scholar]
  15. Girgis, H. S., Liu, Y., Ryu, W. S. & Tavazoie, S. ( 2007; ). A comprehensive genetic characterization of bacterial motility. PLoS Genet 3, 1644–1660.
    [Google Scholar]
  16. Green, J. & Paget, M. S. ( 2004; ). Bacterial redox sensors. Nat Rev Microbiol 2, 954–966.[CrossRef]
    [Google Scholar]
  17. Green, J., Crack, J. C., Thomson, A. J. & Le Brun, N. E. ( 2009; ). Bacterial sensors of oxygen. Curr Opin Microbiol 12, 145–151.[CrossRef]
    [Google Scholar]
  18. Harshey, R. M. & Matsuyama, T. ( 1994; ). Dimorphic transition in Escherichia coli and Salmonella typhimurium: surface-induced differentiation into hyperflagellate swarmer cells. Proc Natl Acad Sci U S A 91, 8631–8635.[CrossRef]
    [Google Scholar]
  19. Hecht, G. B. & Newton, A. ( 1995; ). Identification of a novel response regulator required for the swarmer-to-stalked cell transition in Caulobacter crescentus. J Bacteriol 177, 6223–6229.
    [Google Scholar]
  20. Hisert, K. B., MacCoss, M., Shiloh, M. U., Darwin, K. H., Singh, S., Jones, R. A., Ehrt, S., Zhang, Z., Gaffney, B. L. & other authors ( 2005; ). A glutamate-alanine-leucine (EAL) domain protein of Salmonella controls bacterial virulence in mice, anti-oxidant defence and killing of macrophages: role of cyclic-diGMP. Mol Microbiol 56, 1234–1245.[CrossRef]
    [Google Scholar]
  21. Hoffmann, K. & Stoffel, W. ( 1993; ). TMbase – a database of membrane spanning protein segments. Biol Chem Hoppe Seyler 374, 166.
    [Google Scholar]
  22. Jenal, U. ( 2004; ). Cyclic diguanosine monophosphate comes of age: a novel secondary messenger involved in modulating cell surface structures in bacteria? Curr Opin Microbiol 7, 185–191.[CrossRef]
    [Google Scholar]
  23. Jenal, U. & Malone, J. ( 2006; ). Mechanisms of cyclic-di-GMP signalling in bacteria. Annu Rev Genet 40, 385–407.[CrossRef]
    [Google Scholar]
  24. Jervis, A. J. & Green, J. ( 2007; ). In vivo demonstration of FNR dimers in response to lower O2 availability. J Bacteriol 189, 2930–2932.[CrossRef]
    [Google Scholar]
  25. Kang, Y., Durfee, T., Glasner, J. D., Qiu, Y., Frisch, D., Winterberg, K. M. & Blattner, F. R. ( 2004; ). Systematic mutagenesis of the Escherichia coli genome. J Bacteriol 186, 4921–4930.[CrossRef]
    [Google Scholar]
  26. Kang, Y., Weber, K. D., Qiu, Y., Kiley, P. J. & Blattner, F. R. ( 2005; ). Genome-wide expression analysis indicates that FNR of Escherichia coli K-12 regulates a large number of genes of unknown function. J Bacteriol 187, 1135–1160.[CrossRef]
    [Google Scholar]
  27. Kehres, D. G., Zaharik, M. L., Finlay, B. B. & Maguire, M. E. ( 2000; ). The NRAMP proteins of Salmonella typhimurium and Escherichia coli are selective manganese transporters involved in the response to reactive oxygen. Mol Microbiol 36, 1085–1100.[CrossRef]
    [Google Scholar]
  28. Kulasakara, H., Lee, V., 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 phosphodiesterases reveals a role for bis-(3′–5′)-cyclic-GMP in virulence. Proc Natl Acad Sci U S A 103, 2839–2844.[CrossRef]
    [Google Scholar]
  29. Lazazzera, B. A., Beinert, H., Khoroshilova, N., Kennedy, M. C. & Kiley, P. J. ( 1996; ). DNA binding and dimerization of the Fe-S-containing FNR protein from Escherichia coli are regulated by oxygen. J Biol Chem 271, 2762–2768.[CrossRef]
    [Google Scholar]
  30. Lee, V. T., Matewish, J. M., Kessler, J. L., Hyodo, M., Hayakowa, Y. & Lory, S. ( 2007; ). A cyclic-di-GMP receptor required for bacterial exopolysaccharide production. Mol Microbiol 65, 1474–1484.[CrossRef]
    [Google Scholar]
  31. Lennox, E. S. ( 1955; ). Transduction of linked genetic characters of the host by bacteriophage P1. Virology 1, 190–206.[CrossRef]
    [Google Scholar]
  32. Martinez, E., Bartolome, B. & Delacruz, F. ( 1988; ). pACYC184-derived cloning vectors containing the multiple cloning site and lacZα reporter gene of pUC8/9 and pUC18/19 plasmids. Gene 68, 159–162.[CrossRef]
    [Google Scholar]
  33. Medicis, E. D., Paquette, J., Gauthier, J. J. & Shapcott, D. ( 1986; ). Magnesium and manganese content of halophilic bacteria. Appl Environ Microbiol 52, 567–573.
    [Google Scholar]
  34. Meng, W., Green, J. & Guest, J. R. ( 1997; ). FNR-dependent repression of ndh gene expression requires two upstream FNR-binding sites. Microbiology 143, 1521–1532.[CrossRef]
    [Google Scholar]
  35. Miller, J. H. ( 1972; ). Assay of β-galactosidase. In Experiments in Molecular Genetics, pp. 352–355. Edited by Miller, J. H.. Cold Spring Harbor, NY. : Cold Spring Harbor Laboratory.
    [Google Scholar]
  36. Nikolskaya, A. N., Mulkidjanian, A. Y., Beech, I. B. & Galperin, M. Y. ( 2003; ). MASE1 and MASE2: two novel integral membrane sensory domains. J Mol Microbiol Biotechnol 5, 11–16.[CrossRef]
    [Google Scholar]
  37. Partridge, J. D., Scott, C., Tang, Y., Poole, R. K. & Green, J. ( 2006; ). Escherichia coli transcriptome dynamics during the transition from anaerobic to aerobic conditions. J Biol Chem 281, 27806–27815.[CrossRef]
    [Google Scholar]
  38. Partridge, J. D., Poole, R. K. & Green, J. ( 2007a; ). The Escherichia coli yhjA gene, encoding a predicted cytochrome c peroxidase, is regulated by FNR and OxyR. Microbiology 153, 1499–1509.[CrossRef]
    [Google Scholar]
  39. Partridge, J. D., Sanguinetti, G., Dibden, D. P., Roberts, R. E., Poole, R. K. & Green, J. ( 2007b; ). Transition of Escherichia coli from aerobic to micro-aerobic conditions involves fast and slow reacting regulatory components. J Biol Chem 282, 11230–11237.[CrossRef]
    [Google Scholar]
  40. Paul, R., Weiser, S., Amiot, N. C., 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]
  41. Paul, R., Abel, S., Wassmann, P., Beck, A., Heerklotz, H. & Jenal, U. ( 2007; ). Activation of the diguanylate cyclase PleD by phosphorylation-mediated dimerization. J Biol Chem 282, 29170–29177.[CrossRef]
    [Google Scholar]
  42. Pei, J. & Grishin, N. V. ( 2001; ). GGDEF domain is homologous to adenylyl cyclase. Proteins 42, 210–216.[CrossRef]
    [Google Scholar]
  43. Pesavento, C. & Hengge, R. ( 2009; ). Bacterial nucleotide-based second messengers. Curr Opin Microbiol 12, 170–176.[CrossRef]
    [Google Scholar]
  44. 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]
  45. Poteete, A. R. & Fenton, A. C. ( 1984; ). λ red-dependent growth and recombination of phage P22. Virology 134, 161–167.[CrossRef]
    [Google Scholar]
  46. 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]
  47. Römling, U. & Amikam, D. ( 2006; ). Cyclic-di-GMP as a second messenger. Curr Opin Microbiol 9, 218–228.[CrossRef]
    [Google Scholar]
  48. Ross, P., Weinhouse, H., Aloni, Y., Michaeli, D., Weinburger-Ohana, P., Mayer, R., Braun, S., de Vroom, E., van der Marel, G. A. & other authors ( 1987; ). Regulation of cellulose synthesis in Acetobacter xylinum by cyclic diguanylate. Nature 325, 279–281.[CrossRef]
    [Google Scholar]
  49. Ryan, R. P., Fouhy, Y., Lucey, J. F. & Dow, J. M. ( 2006; ). Cyclic-di-GMP signalling in bacteria: recent advances and new puzzles. J Bacteriol 188, 8327–8334.[CrossRef]
    [Google Scholar]
  50. Ryjenkov, D. A., Tarutina, M., Moskvin, O. M. & 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]
  51. 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 domain protein YcgR controls motility in enterobacteria. J Biol Chem 281, 30310–30314.[CrossRef]
    [Google Scholar]
  52. Salmon, K., Hung, S. P., Mekjian, K., Baldi, P., Hatfield, G. W. & Gunsalus, R. P. ( 2003; ). Global gene expression profiling in Escherichia coli K12: the effects of oxygen availability and FNR. J Biol Chem 278, 29837–29855.[CrossRef]
    [Google Scholar]
  53. Sambrook, J. W. & Russell, D. W. ( 2001; ). Molecular Cloning: a Laboratory Manual, 3rd edn. Cold Spring Harbor, NY. : Cold Spring Harbor Laboratory.
    [Google Scholar]
  54. Sasakura, Y., Hirata, S., Sugiyama, S., Suzuki, S., Taguchi, S., Watanabe, M., Matsui, T., Sagami, I. & Shimizu, T. ( 2002; ). Characterization of a direct oxygen sensor heme protein from Escherichia coli. Effects of heme redox states and mutations at the heme binding site on catalysis and structure. J Biol Chem 277, 23821–23827.[CrossRef]
    [Google Scholar]
  55. Schmidt, A. J., Ryjenkov, D. A. & Gomelsky, M. ( 2005; ). Ubiquitous protein domain EAL encodes cyclic diguanylate-specific phosphodiesterase: enzymatically active and inactive EAL domains. J Bacteriol 187, 4774–4781.[CrossRef]
    [Google Scholar]
  56. 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]
  57. 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]
  58. 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 signalling network in Salmonella. Proc Natl Acad Sci U S A 106, 7997–8002.[CrossRef]
    [Google Scholar]
  59. Sommerfeldt, N., Possling, A., Becker, G., Pesavento, C., Tschowri, N. & Hengge, R. ( 2009; ). Gene expression patterns and differential input into curli fimbriae regulation of all GGDEF/EAL domain proteins in Escherichia coli. Microbiology 155, 1318–1331.[CrossRef]
    [Google Scholar]
  60. Sonnhammer, E. L., von Heijne, G. & Krogh, A. ( 1998; ). A hidden Markov model for predicting transmembrane helices in protein sequences. Proc Int Conf Intell Syst Mol Biol 6, 175–182.
    [Google Scholar]
  61. Spiro, S. & Guest, J. R. ( 1987; ). Regulation and over-expression of the fnr gene of Escherichia coli. J Gen Microbiol 133, 3279–3288.
    [Google Scholar]
  62. Suzuki, K., Babitzke, P., Kushner, S. R. & Romeo, T. ( 2006; ). Identification of a novel regulatory protein (CsrD) that targets the global regulator RNAs CsrB and CsrC for degradation by RNase E. Genes Dev 20, 2605–2617.[CrossRef]
    [Google Scholar]
  63. Tal, R., Wong, H. C., Calhoon, R., Gelfand, D., Fear, A. L., Volman, G., Mayer, R., Ross, P., Amikan, D. & other authors ( 1998; ). Three cdg operons control cellular turnover of cyclic-di-GMP in Acetobacter xylinum: genetic organization and occurrence of conserved domains in isoenzymes. J Bacteriol 180, 4416–4425.
    [Google Scholar]
  64. 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]
  65. Tanaka, A., Takahashi, H. & Shimizu, T. ( 2007; ). Critical role of the heme axial ligand, Met95, in locking catalysis of the phosphodiesterase from Escherichia coli (Ec DOS) toward cyclic diGMP. J Biol Chem 282, 21301–21307.[CrossRef]
    [Google Scholar]
  66. Tischler, A. D. & Camilli, A. ( 2004; ). Cyclic diguanylate (c-di-GMP) regulates Vibrio cholerae biofilm formation. Mol Microbiol 53, 857–869.[CrossRef]
    [Google Scholar]
  67. Tischler, A. D. & Camilli, A. ( 2005; ). Cyclic diguanylate regulates Vibrio cholerae virulence gene expression. Infect Immun 73, 5873–5882.[CrossRef]
    [Google Scholar]
  68. Tuckerman, J. R., Gonzalez, G., Sousa, E. H., Wan, X., Saito, J. A., Alam, M. & Gilles-Gonzalez, M.-A. ( 2009; ). An oxygen-sensing diguanylate cyclase and phosphodiesterase couple for c-di-GMP control. Biochemistry 48, 9764–9774.[CrossRef]
    [Google Scholar]
  69. Unden, G., Achebach, S., Holighaus, G., Tran, H.-Q., Wackwitz, B. & Zeuner, Y. ( 2002; ). Control of FNR function of Escherichia coli by O2 and reducing conditions. J Mol Microbiol Biotechnol 4, 263–268.
    [Google Scholar]
  70. Wing, H. J., Williams, S. M. & Busby, S. J. W. ( 1995; ). Spacing requirements for transcription activation by Escherichia coli FNR protein. J Bacteriol 177, 6704–6710.
    [Google Scholar]
  71. Xiong, J., Kurtz, D. M., Jr, Ai, J. & Sanders-Loehr, J. ( 2000; ). A hemerythrin-like domain in a bacterial chemotaxis protein. Biochemistry 39, 5117–5125.[CrossRef]
    [Google Scholar]
  72. Yu, D., Ellis, H. M., Lee, E.-C., Jenkins, N. A., Copeland, N. G. & Court, D. L. ( 2000; ). An efficient recombination system for chromosome engineering in Escherichia coli. Proc Natl Acad Sci U S A 97, 5978–5983.[CrossRef]
    [Google Scholar]
  73. Ziegelhoffer, E. C. & Kiley, P. J. ( 1995; ). In vitro analysis of a constitutively active mutant form of the Escherichia coli global transcription factor FNR. J Mol Biol 245, 351–361.[CrossRef]
    [Google Scholar]
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