Virulence and prodigiosin antibiotic biosynthesis in Serratia are regulated pleiotropically by the GGDEF/EAL domain protein, PigX

Journal of Bacteriology

Volumn 189, Issue 21, 2007, Pages 7653-7662

  Fineran, Peter C ^a   Williamson, Neil R ^a   Lilley, Kathryn S ^a   Salmond, George P C ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; CARBAPENEM; CELLULASE; CYCLIC GMP PHOSPHODIESTERASE; DNA; GENE PRODUCT; GLUTAMYLALANYLLEUCYL DOMAIN PROTEIN; GLYCYLGLYCYLASPARTYLGLUTAMYLPHENYLALANYL DOMAIN PROTEIN; POLYGALACTURONASE; PRODIGIOSIN; PROTEIN PIGX; UNCLASSIFIED DRUG;

ANTIBACTERIAL ACTIVITY; ANTIBIOTIC BIOSYNTHESIS; ARTICLE; BACTERIAL VIRULENCE; BINDING SITE; BIOFILM; CELL WALL; DIMERIZATION; DRUG SYNTHESIS; ENZYME DEGRADATION; GENE MUTATION; NONHUMAN; NUCLEOTIDE SEQUENCE; OPERON; OPPORTUNISTIC INFECTION; PIGX GENE; PLEIOTROPY; PREDICTION; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DETERMINATION; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN MOTIF; QUANTITATIVE ANALYSIS; REGULATOR GENE; SECOND MESSENGER; SEQUENCE ANALYSIS; SERRATIA; TRANSCRIPTION INITIATION; TRANSCRIPTION REGULATION; VALIDATION PROCESS;

AMINO ACID SEQUENCE; BACTERIAL PROTEINS; DNA PRIMERS; MOVEMENT; PHOSPHORIC DIESTER HYDROLASES; PRODIGIOSIN; SERRATIA; VIRULENCE;

HEXAPODA; NEGIBACTERIA; SERRATIA; SERRATIA SP.; SUIDAE;

EID: 35648979519     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.00671-07     Document Type: Article

References (57)

1. Alban, A., S. O. David, L. Bjorkesten, C. Andersson, E. Sloge, S. Lewis, and I. Currie. 2003. A novel experimental design for comparative two-dimensional gel analysis: two-dimensional difference gel electrophoresis incorporating a pooled internal standard. Proteomics 3:36-44.
2. Altschul, S. F., T. L. Madden, A. A. Schaffer, J. Zhang, Z. Zhang, W. Miller, and D. J. Lipman. 1997. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25:3389-3402.
3. Amikam, D., and M. Y. Galperin. 2006. PilZ domain is part of the bacterial c-di-GMP binding protein. Bioinformatics 22:3-6.
4. Andro, T., J. P. Chambost, A. Kotoujansky, J. Cattaneo, Y. Bertheau, F. Barras, F. Van Gijsegem, and A. Coleno. 1984. Mutants of Erwinia chrysanthemi defective in secretion of pectinase and cellulase. J. Bacteriol. 160:1199-1203.
5. Bochner, B. R., and B. N. Ames. 1982. Complete analysis of cellular nucleotides by two-dimensional thin layer chromatography. J. Biol. Chem. 257:9759-9769.
6. Bohin, J. P. 2000. Osmoregulated periplasmic glucans in Proteobacteria. FEMS Microbiol. Lett. 186:11-19.
7. Bouchart, F., A. Delangle, J. Lemoine, J. P. Bohin, and J. M. Lacroix. 2007. Proteomic analysis of a nonvirulent mutant of the phytopathogenic bacterium Erwinia chrysanthemi deficient in osmoregulated periplasmic glucans: change in protein expression is not restricted to the envelope, but affects general metabolism. Microbiology 153:760-767.
8. Burr, T., A. M. L. Barnard, M. J. Corbett, C. L. Pemberton, N. J. Simpson, and G. P. C. Salmond. 2006. Identification of the central quorum sensing regulator of virulence in the enteric phytopathogen, Erwinia carotovora: the VirR repressor. Mol. Microbiol. 59:113-125.
9. Chandu, D., and D. Nandi. 2003. PepN is the major aminopeptidase in Escherichia coli: insights on substrate specificity and role during sodium-salicylate-induced stress. Microbiology 149:3437-3447.
10. Christen, B., M. Christen, R. Paul, F. Schmid, M. Folcher, P. Jenoe, M. Meuwly, and U. Jenal. 2006. Allosteric control of cyclic di-GMP signaling. J. Biol. Chem. 281:32015-32024.
11. Christen, M., B. Christen, M. G. Allan, M. Folcher, P. Jeno, S. Grzesiek, and U. Jenal. 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.
12. Christen, M., B. Christen, M. Folcher, A. Schauerte, and U. Jenal. 2005. Identification and characterization of a cyclic di-GMP-specific phosphodiesterase and its allosteric control by GTP. J. Biol. Chem. 280:30829-30837.
13. Cogez, V., P. Talaga, J. Lemoine, and J. P. Bohin. 2001. Osmoregulated periplasmic glucans of Erwinia chrysanthemi. J. Bacteriol. 183:3127-3133.
14. Coulthurst, S. J., A. M. Barnard, and G. P. Salmond. 2005. Regulation and biosynthesis of carbapenem antibiotics in bacteria. Nat. Rev. Microbiol. 3:295-306.
15. Coulthurst, S. J., C. L. Kurz, and G. P. Salmond. 2004. luxS mutants of Serratia defective in autoinducer-2-dependent "quorum sensing" show strain-dependent impacts on virulence and production of carbapenem and prodigiosin. Microbiology 150:1901-1910.
16. Coulthurst, S. J., K. S. Lilley, and G. P. C. Salmond. 2006. Genetic and proteomic analysis of the role of luxS in the enteric phytopathogen, Erwinia carotovora. Mol. Plant Pathol. 7:31-45.
17. Crow, M. A. 2001. Ph.D. thesis. The University of Cambridge, Cambridge, United Kingdom.
18. de Lorenzo, V., M. Herrero, U. Jakubzik, and K. N. Timmis. 1990. Mini-Tn5 transposon derivatives for insertion mutagenesis, promoter probing, and chromosomal insertion of cloned DNA in gram-negative eubacteria. J. Bacteriol. 172:6568-6572.
19. Fineran, P. C., L. Everson, H. Slater, and G. P. Salmond. 2005. A GntR family transcriptional regulator (PigT) controls gluconate-mediated repression and defines a new, independent pathway for regulation of the tripyrrole antibiotic, prodigiosin, in Serratia. Microbiology 151:3833-3845.
20. Fineran, P. C., H. Slater, L. Everson, K. Hughes, and G. P. Salmond. 2005. Biosynthesis of tripyrrole and beta-lactam secondary metabolites in Serratia: integration of quorum sensing with multiple new regulatory components in the control of prodigiosin and carbapenem antibiotic production. Mol. Microbiol. 56:1495-1517.
21. Galperin, M. Y. 2004. Bacterial signal transduction network in a genomic perspective. Environ. Microbiol. 6:552-567.
22. Grimont, P. A., and F. Grimont. 1978. The genus Serratia. Annu. Rev. Microbiol. 32:221-248.
23. Harley, C. B., and R. P. Reynolds. 1987. Analysis of E. coli promoter sequences. Nucleic Acids Res. 15:2343-2361.
24. Harris, A. K., N. R. Williamson, H. Slater, A. Cox, S. Abbasi, I. Foulds, H. T. Simonsen, F. J. Leeper, and G. P. Salmond. 2004. The Serratia gene cluster encoding biosynthesis of the red antibiotic, prodigiosin, shows species- and strain-dependent genome context variation. Microbiology 150:3547-3560.
25. Hejazi, A., and F. R. Falkiner. 1997. Serratia marcescens. J. Med. Microbiol. 46:903-912.
26. Hickman, J. W., D. F. Tifrea, and C. S. Harwood. 2005. A chemosensory System that regulates biofilm formation through modulation of cyclic diguanylate levels. Proc. Natl. Acad. Sci. USA 102:14422-14427.
27. Hisert, K. B., M. MacCoss, M. U. Shiloh, K. H. Darwin, S. Singh, R. A. Jones, S. Ehrt, Z. Zhang, B. L. Gaffney, S. Gandotra, D. W. Holden, D. Murray, and C. Nathan. 2005. A glutamate-alanine-leucine (EAL) domain protein of Salmonella controls bacterial survival in mice, antioxidant defense and killing of macrophages: role of cyclic diGMP. Mol. Microbiol. 56:1234-1245.
28. Hoang, T. T., and H. P. Schweizer. 1999. Characterization of Pseudomonas aeruginosa enoyl-acyl carrier protein reductase (FabI): a target for the antimicrobial triclosan and its role in acylated homoserine lactone synthesis. J. Bacteriol. 181:5489-5497.
29. Hoffman, L. R., D. A. D'Argenio, M. J. MacCoss, Z. Zhang, R. A. Jones, and S. I. Miller. 2005. Aminoglycoside antibiotics induce bacterial biofilm formation. Nature 436:1171-1175.
30. Hood, D. W., R. Heidstra, U. K. Swoboda, and D. A. Hodgson. 1992. Molecular genetic analysis of proline and tryptophan biosynthesis in Streptomyces coelicolor A3(2): interaction between primary and secondary metabolism - a review. Gene 115:5-12.
31. Jenal, U. 2004. Cyclic di-guanosine-monophosphate comes of age: a novel secondary messenger involved in modulating cell surface structures in bacteria? Curr. Opin. Microbiol. 7:185-191.
32. Jenal, U., and J. Malone. 2006. Mechanisms of cyclic-di-GMP signaling in bacteria. Annu. Rev. Genet. 40:385-407.
33. Kazmierczak, B. I., M. B. Lebron, and T. S. Murray. 2006. Analysis of FimX, a phosphodiesterase that governs twitching motility in Pseudomonas aeruginosa. Mol. Microbiol. 60:1026-1043.
34. Larsen, R. A., M. M. Wilson, A. M. Guss, and W. W. Metcalf. 2002. Genetic analysis of pigment biosynthesis in Xanthobacter autotrophicus Py2 using a new, highly efficient transposon mutagenesis system that is functional in a wide variety of bacteria. Arch. Microbiol. 178:193-201.
35. Mendez-Ortiz, M. M., M. Hyodo, Y. Hayakawa, and J. Membrillo-Hernandez. 2006. Genome-wide transcriptional profile of Escherichia coli in response to high levels of the second messenger 3′,5′-cyclic diguanylic acid. J. Biol. Chem. 281:8090-8099.
36. Mikkelsen, H., Z. Duck, K. S. Lilley, and M. Welch. 2007. Interrelationships between colonies, biofilms, and planktonic cells of Pseudomonas aeruginosa. J. Bacteriol. 189:2411-2416.
37. Neidhardt, F. C., J. L. Ingraham, K. B. Low, B. Magasanik, and M. Schlechter (ed.). 1987. Escherichia coli and Salmonella typhimurium: cellular and molecular biology, 1st ed. American Society for Microbiology, Washington, DC.
38. Page, F., S. Altabe, N. Hugouvieux-Cotte-Pattat, J. M. Lacroix, J. Robert-Baudouy, and J. P. Bohin. 2001. Osmoregulated periplasmic glucan synthesis is required for Erwinia chrysanthemi pathogenicity. J. Bacteriol. 183:3134-3141.
39. Parker, W. L., M. L. Rathnum, J. S. Wells, Jr., W. H. Trejo, P. A. Principe, and R. B. Sykes. 1982. SQ 27,860, a simple carbapenem produced by species of Serratia and Erwinia. J. Antibiot. (Tokyo) 35:653-660.
40. Paul, R., S. Weiser, N. C. Amiot, C. Chan, T. Schirmer, B. Giese, and U. Jenal. 2004. Cell cycle-dependent dynamic localization of a bacterial response regulator with a novel di-guanylate cyclase output domain. Genes Dev. 18:715-727.
41. Romling, U., and D. Amikam. 2006. Cyclic di-GMP as a second messenger. Curr. Opin. Microbiol. 9:218-228.
42. Ryan, R. P., Y. Fouhy, J. F. Lucey, and J. M. Dow. 2006. Cyclic di-GMP signaling in bacteria: recent advances and new puzzles. J. Bacteriol. 188: 8327-8334.
43. Ryjenkov, D. A., R. Simm, U. Romling, and M. Gomelsky. 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.
44. Ryjenkov, D. A., M. Tarutina, O. V. Moskvin, and M. Gomelsky. 2005. Cyclic diguanylate is a ubiquitous signaling molecule in bacteria: insights into biochemistry of the GGDEF protein domain. J. Bacteriol. 187:1792-1798.
45. Sambrook, J., E. F. Fritsch, and T. Maniatis. 1989. Molecular cloning: a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
46. Schmidt, A. J., D. A. Ryjenkov, and M. Gomelsky. 2005. The ubiquitous protein domain EAL is a cyclic diguanylate-specific phosphodiesterase: enzymatically active and inactive EAL domains. J. Bacteriol. 187:4774-4781.
47. Slater, H., M. Crow, L. Everson, and G. P. Salmond. 2003. Phosphate availability regulates biosynthesis of two antibiotics, prodigiosin and carbapenem, in Serratia via both quorum-sensing-dependent and -independent pathways. Mol. Microbiol. 47:303-320.
48. Stock, I., T. Grueger, and B. Wiedemann. 2003. Natural antibiotic susceptibility of strains of Serratia marcescens and the S. liquefaciens complex: S. liquefaciens sensu stricto, S. proteamaculans and S. grimesii. Int. J. Antimicrob. Agents 22:35-47.
49. Suzuki, K., P. Babitzke, S. R. Kushner, and T. Romeo. 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.
50. Tamayo, R., A. D. Tischler, and A. Camilli. 2005. The EAL domain protein VieA is a cyclic diguanylate phosphodiesterase. J. Biol. Chem. 280:33324-33330.
51. Thomson, N. R., M. A. Crow, S. J. McGowan, A. Cox, and G. P. Salmond. 2000. Biosynthesis of carbapenem antibiotic and prodigiosin pigment in Serratia is under quorum sensing control. Mol. Microbiol. 36:539-556.
52. Tischler, A. D., and A. Camilli. 2004. Cyclic diguanylate (c-di-GMP) regulates Vibrio cholerae biofilm formation. Mol. Microbiol. 53:857-869.
53. Tischler, A. D., and A. Camilli. 2005. Cyclic diguanylate regulates Vibrio cholerae virulence gene expression. Infect. Immun. 73:5873-5882.
54. Wasserman, H. H., R. J. Skies, P. Peverada, C. K. Shaw, R. J. Cushley, and C. R. Lipsky. 1973. Biosynthesis of prodigiosin. Incorporation patterns of C-labeled alanine, proline, glycine, and serine elucidated by Fourier transform nuclear magnetic resonance. J. Am. Chem. Soc. 95:6874-6875.
55. Whitehead, N. A., A. M. Barnard, H. Slater, N. J. Simpson, and G. P. Salmond. 2001. Quorum-sensing in gram-negative bacteria. FEMS Microbiol. Rev. 25:365-404.
56. Williamson, N. R., P. C. Fineran, F. J. Leeper, and G. P. Salmond. 2006. The biosynthesis and regulation of bacterial prodiginines. Nat. Rev. Microbiol. 4:887-899.
57. Williamson, N. R., H. T. Simonsen, R. A. Ahmed, G. Goldet, H. Slater, L. Woodley, F. J. Leeper, and G. P. Salmond. 2005. Biosynthesis of the red antibiotic, prodigiosin, in Serratia: identification of a novel 2-methyl-3-n-amyl-pyrrole (MAP) assembly pathway, definition of the terminal condensing enzyme, and implications for undecylprodigiosin biosynthesis in Streptomyces. Mol. Microbiol. 56:971-989.