GIL, a new c-di-GMP-binding protein domain involved in regulation of cellulose synthesis in enterobacteria

Molecular Microbiology

Volumn 93, Issue 3, 2014, Pages 439-452

  Fang, Xin ^a   Ahmad, Irfan ^b   Blanka, Andrea ^b   Schottkowski, Marco ^b   Cimdins, Annika ^b   Galperin, Michael Y ^c   Römling, Ute ^b   Gomelsky, Mark ^a  

^a UNIVERSITY OF WYOMING   (United States)

^b KAROLINSKA INSTITUTE   (Sweden)

^c NATIONAL INSTITUTES OF HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELLULOSE; CYCLIC DI GMP RECEPTOR BCSA; CYCLIC DI GMP RECEPTOR BCSE; CYCLIC DI GMP RECEPTOR ILVH; CYCLIC DI GMP RECEPTOR RIMO; RECEPTOR; UNCLASSIFIED DRUG; BACTERIAL PROTEIN; BIS(3',5')-CYCLIC DIGUANYLIC ACID; CELLULOSE SYNTHASE; CYCLIC GMP; DIGUANYLATE CYCLASE; ESCHERICHIA COLI PROTEIN; GLUCOSYLTRANSFERASE; GLYCOSYLTRANSFERASE; LYASE; PROTEIN BINDING;

ARTICLE; BACTERIAL GENE; BCSE GENE; BETAPROTEOBACTERIA; BINDING SITE; BIOASSAY; BIOSYNTHESIS; CONTROLLED STUDY; DIFFERENTIAL RADIAL CAPILLARY ACTION OF LIGAND ASSAY; ENTEROBACTERIACEAE; ESCHERICHIA COLI; GAMMAPROTEOBACTERIA; GENE DELETION; GENE LIBRARY; GENETIC SCREENING; GGDEF I SITE LIKE DOMAIN; IN VIVO STUDY; KLEBSIELLA PNEUMONIAE; MUTATIONAL ANALYSIS; NONHUMAN; OPERON; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN MOTIF; PROTEIN PURIFICATION; RECEPTOR BINDING; SALMONELLA ENTERICA; SENSITIVITY ANALYSIS; SIGNAL TRANSDUCTION; STRUCTURE ACTIVITY RELATION; ANALOGS AND DERIVATIVES; CHEMISTRY; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; SALMONELLA ENTERICA SEROVAR TYPHIMURIUM; SITE DIRECTED MUTAGENESIS;

BACTERIAL PROTEINS; CELLULOSE; CYCLIC GMP; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; GENE EXPRESSION REGULATION, BACTERIAL; GLUCOSYLTRANSFERASES; GLYCOSYLTRANSFERASES; KLEBSIELLA PNEUMONIAE; MUTAGENESIS, SITE-DIRECTED; OPERON; PHOSPHORUS-OXYGEN LYASES; PROTEIN BINDING; PROTEIN INTERACTION DOMAINS AND MOTIFS; SALMONELLA TYPHIMURIUM; SIGNAL TRANSDUCTION;

EID: 84904859048     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/mmi.12672     Document Type: Article

References (63)

1. Altschul, S.F., Madden, T.L., Schaffer, A.A., Zhang, J., Zhang, Z., Miller, W., and Lipman, D.J. (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25: 3389-3402.
2. Amikam, D., and Galperin, M.Y. (2006) PilZ domain is part of the bacterial c-di-GMP binding protein. Bioinformatics 22: 3-6.
3. Barends, T.R., Hartmann, E., Griese, J.J., Beitlich, T., Kirienko, N.V., Ryjenkov, D.A., etal. (2009) Structure and mechanism of a bacterial light-regulated cyclic nucleotide phosphodiesterase. Nature 459: 1015-1018.
4. Boehm, A., Kaiser, M., Li, H., Spangler, C., Kasper, C.A., Ackermann, M., etal. (2010) Second messenger-mediated adjustment of bacterial swimming velocity. Cell 141: 107-116.
5. Brombacher, E., Baratto, A., Dorel, C., and 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.
6. Chan, C., Paul, R., Samoray, D., Amiot, N.C., Giese, B., Jenal, U., and Schirmer, T. (2004) Structural basis of activity and allosteric control of diguanylate cyclase. Proc Natl Acad Sci USA 101: 17084-17089.
7. Christen, M., Christen, B., Allan, M.G., Folcher, M., Jeno, P., Grzesiek, S., and 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 USA 104: 4112-4117.
8. Cole, C., Barber, J.D., and Barton, G.J. (2008) The Jpred 3secondary structure prediction server. Nucleic Acids Res 36: W197-W201.
9. Corrigan, R.M., Campeotto, I., Jeganathan, T., Roelofs, K.G., Lee, V.T., and Grundling, A. (2013) Systematic identification of conserved bacterial c-di-AMP receptor proteins. Proc Natl Acad Sci USA 110: 9084-9089.
10. Datsenko, K.A., and Wanner, B.L. (2000) One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc Natl Acad Sci USA 97: 6640-6645.
11. Düvel, J., Bertinetti, D., Möller, S., Schwede, F., Morr, M., Wissing, J., etal. (2012) A chemical proteomics approach to identify c-di-GMP binding proteins in Pseudomonas aeruginosa. J Microbiol Methods 88: 229-236.
12. Fang, X., and Gomelsky, M. (2010) A post-translational, c-di-GMP-dependent mechanism regulating flagellar motility. Mol Microbiol 76: 1295-1305.
13. Finn, R.D., Clements, J., and Eddy, S.R. (2011) HMMER web server: interactive sequence similarity searching. Nucleic Acids Res 39: W29-W37.
14. Grantcharova, N., Peters, V., Monteiro, C., Zakikhany, K., and Römling, U. (2010) Bistable expression of CsgD in biofilm development of Salmonella enterica serovar Typhimurium. J Bacteriol 192: 456-466.
15. Guzman, L.M., Belin, D., Carson, M.J., and Beckwith, J. (1995) Tight regulation, modulation, and high-level expression by vectors containing the arabinose PBAD promoter. J Bacteriol 177: 4121-4130.
16. Hu, J., Wang, B., Fang, X., Means, W.J., McCormick, R.J., Gomelsky, M., and Zhu, M.J. (2013) c-di-GMP signaling regulates E. coli O157:H7 adhesion to colonic epithelium. Vet Microbiol 164: 344-351.
17. Jahn, C.E., Selimi, D.A., Barak, J.D., and Charkowski, A.O. (2011) The Dickeya dadantii biofilm matrix consists of cellulose nanofibres, and is an emergent property dependent upon the type III secretion system and the cellulose synthesis operon. Microbiology 157: 2733-2744.
18. Karlinsey, J.E. (2007) Lambda-Red genetic engineering in Salmonella enterica serovar Typhimurium. Methods Enzymol 421: 199-209.
19. Khan, S.R., Gaines, J., Roop, R.M., 2nd, and Farrand, S.K. (2008) Broad-host-range expressionvectors with tightly regulated promoters and their use to examine the influence of TraR and TraM expression on Ti plasmid quorum sensing. Appl Environ Microbiol 74: 5053-5062.
20. Kitagawa, M., Ara, T., Arifuzzaman, M., Ioka-Nakamichi, T., Inamoto, E., Toyonaga, H., and Mori, H. (2005) Complete set of ORF clones of Escherichia coli ASKA library (a complete set of E. coli K-12 ORF archive): unique resources for biological research. DNA Res 12: 291-299.
21. Krasteva, P.V., Fong, J.C., Shikuma, N.J., Beyhan, S., Navarro, M.V., Yildiz, F.H., and Sondermann, H. (2010) Vibrio cholerae VpsT regulates matrix production and motility by directly sensing cyclic di-GMP. Science 327: 866-868.
22. Lacey, M.M., Partridge, J.D., and Green, J. (2010) Escherichia coli K-12 YfgF is an anaerobic cyclic di-GMP phosphodiesterase with roles in cell surface remodelling and the oxidative stress response. Microbiology 156: 2873-2886.
23. Le Quere, B., and Ghigo, J.M. (2009) BcsQ is an essential component of the Escherichia coli cellulose biosynthesis apparatus that localizes at the bacterial cell pole. Mol Microbiol 72: 724-740.
24. Leduc, J.L., and Roberts, G.P. (2009) Cyclic di-GMP allosterically inhibits the CRP-like protein (Clp) of Xanthomonas axonopodis pv. citri. J Bacteriol 191: 7121-7122.
25. Lindenberg, S., Klauck, G., Pesavento, C., Klauck, E., and 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: 2001-2014.
26. Ma, Q., Zhang, G., and Wood, T.K. (2011) Escherichia coli BdcA controls biofilm dispersal in Pseudomonas aeruginosa and Rhizobium meliloti. BMC Res Notes 4: 447.
27. McGuffin, L.J., and Jones, D.T. (2003) Improvement of the GenTHREADER method for genomic fold recognition. Bioinformatics 19: 874-881.
28. Marchler-Bauer, A., and Bryant, S.H. (2004) CD-Search: protein domain annotations on the fly. Nucleic Acids Res 32: W327-W331.
29. Morgan, J.L., Strumillo, J., and Zimmer, J. (2013) Crystallographic snapshot of cellulose synthesis and membrane translocation. Nature 493: 181-186.
30. Nesper, J., Reinders, A., Glatter, T., Schmidt, A., and Jenal, U. (2012) A novel capture compound for the identification and analysis of cyclic di-GMP binding proteins. J Proteomics 75: 4874-4878.
31. Paul, K., Nieto, V., Carlquist, W.C., Blair, D.F., and Harshey, R.M. (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: 128-139.
32. Pesavento, C., Becker, G., Sommerfeldt, N., Possling, A., Tschowri, N., Mehlis, A., and Hengge, R. (2008) Inverse regulatory coordination of motility and curli-mediated adhesion in Escherichia coli. Genes Dev 22: 2434-2446.
33. Povolotsky, T.L., and Hengge, R. (2012) 'Life-style' control networks in Escherichia coli: signaling by the second messenger c-di-GMP. J Biotechnol 160: 10-16.
34. Pultz, I.S., Christen, M., Kulasekara, H.D., Kennard, A., Kulasekara, B., and Miller, S.I. (2012) The response threshold of Salmonella PilZ domain proteins is determined by their binding affinities for c-di-GMP. Mol Microbiol 86: 1424-1440.
35. Punta, M., Coggill, P.C., Eberhardt, R.Y., Mistry, J., Tate, J., Boursnell, C., etal. (2012) The Pfam protein families database. Nucleic Acids Res 40: D290-D301.
36. Roelofs, K.G., Wang, J., Sintim, H.O., and Lee, V.T. (2011) Differential radial capillary action of ligand assay for high-throughput detection of protein-metabolite interactions. Proc Natl Acad Sci USA 108: 15528-15533.
37. Ross, P., Weinhouse, H., Aloni, Y., Michaeli, D., Weinberger-Ohana, P., Mayer, R., etal. (1987) Regulation of cellulose synthesis in Acetobacter xylinum by cyclic diguanylic acid. Nature 325: 279-281.
38. Römling, U. (2002) Molecular biology of cellulose production in bacteria. Res Microbiol 153: 205-212.
39. Römling, U. (2005) Characterization of the rdar morphotype, a multicellular behaviour in Enterobacteriaceae. Cell Mol Life Sci 62: 1234-1246.
40. Römling, U., Sierralta, W.D., Eriksson, K., and Normark, S. (1998) Multicellular and aggregative behaviour of Salmonella typhimurium strains is controlled by mutations in the agfD promoter. Mol Microbiol 28: 249-264.
41. Römling, U., Rohde, M., Olsen, A., Normark, S., and 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.
42. Römling, U., Galperin, M.Y., and Gomelsky, M. (2013) Cyclic di-GMP: the first 25years of a universal bacterial second messenger. Microbiol Mol Biol Rev 77: 1-52.
43. Russell, M.H., Bible, A.N., Fang, X., Gooding, J., Campagna, S., Gomelsky, M., and Alexandre, G. (2013) Integration of the second messenger c-di-GMP into the chemotactic signaling pathway promotes sensory adaptation. mBio 4: e00001-13.
44. Ryjenkov, D.A., Tarutina, M., Moskvin, O.V., and 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.
45. Ryjenkov, D.A., Simm, R., Römling, U., and 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.
46. Sambrook, J., Maniatis, T., and Fritsch, E.F. (1989) Molecular Cloning: A Laboratory Manual, 2nd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
47. Saxena, I.M., Lin, F.C., and Brown, R.M., Jr (1990) Cloning and sequencing of the cellulose synthase catalytic subunit gene of Acetobacter xylinum. Plant Mol Biol 15: 673-683.
48. Schirmer, T., and Jenal, U. (2009) Structural and mechanistic determinants of c-di-GMP signalling. Nat Rev Microbiol 7: 724-735.
49. Schmidt, A.J., Ryjenkov, D.A., and 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.
50. Serra, D.O., Richter, A.M., and Hengge, R. (2013) Cellulose as an architectural element in spatially structured Escherichia coli biofilms. J Bacteriol 195: 5540-5554.
51. Simm, R., Remminghorst, U., Ahmad, I., Zakikhany, K., and 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: 3928-3937.
52. Solano, C., Garcia, B., Valle, J., Berasain, C., Ghigo, J.M., Gamazo, C., and Lasa, I. (2002) Genetic analysis of Salmonella enteritidis biofilm formation: critical role of cellulose. Mol Microbiol 43: 793-808.
53. Söding, J., Biegert, A., and Lupas, A.N. (2005) The HHpred interactive server for protein homology detection and structure prediction. Nucleic Acids Res 33: W244-W248.
54. Standal, R., Iversen, T.G., Coucheron, D.H., Fjaervik, E., Blatny, J.M., and Valla, S. (1994) A new gene required for cellulose production and a gene encoding cellulolytic activity in Acetobacter xylinum are colocalized with the bcs operon. J Bacteriol 176: 665-672.
55. Steiner, S., Lori, C., Boehm, A., and Jenal, U. (2013) Allosteric activation of exopolysaccharide synthesis through cyclic di-GMP-stimulated protein-protein interaction. EMBO J 32: 354-368.
56. Suzuki, K., Babitzke, P., Kushner, S.R., and 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.
57. Tschowri, N., Busse, S., and 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: 522-534.
58. Tuckerman, J.R., Gonzalez, G., and Gilles-Gonzalez, M.A. (2011) Cyclic di-GMP activation of polynucleotide phosphorylase signal-dependent RNA processing. J Mol Biol 407: 633-639.
59. Uzzau, S., Figueroa-Bossi, N., Rubino, S., and Bossi, L. (2001) Epitope tagging of chromosomal genes in Salmonella. Proc Natl Acad Sci USA 98: 15264-15269.
60. 2 factor responsible for nutritional control of the flagellar regulon in Salmonella enterica Serovar Typhimurium. J Bacteriol 193: 1600-1611.
61. 2 factor gene ydiV in Escherichia coli. Microbiology 158: 1533-1542.
62. Wong, H.C., Fear, A.L., Calhoon, R.D., Eichinger, G.H., Mayer, R., Amikam, D., etal. (1990) Genetic organization of the cellulose synthase operon in Acetobacter xylinum. Proc Natl Acad Sci USA 87: 8130-8134.
63. Zogaj, X., Nimtz, M., Rohde, M., Bokranz, W., and Römling, U. (2001) The multicellular morphotypes of Salmonella typhimurium and Escherichia coli produce cellulose as the second component of the extracellular matrix. Mol Microbiol 39: 1452-1463.