Stringent response in Vibrio cholerae: Genetic analysis of spoT gene function and identification of a novel (p)ppGpp synthetase gene

Molecular Microbiology

Volumn 72, Issue 2, 2009, Pages 380-398

  Das, Bhabatosh ^a,b   Pal, Ritesh Ranjan ^a   Bag, Satyabrata ^a   Bhadra, Rupak K ^a  

^a INDIAN INSTITUTE OF CHEMICAL BIOLOGY   (India)

^b CENTRE DE GÉNÉTIQUE MOLÉCULAIRE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

FATTY ACID; GLUCOSE; SYNTHETASE;

ARTICLE; GENE EXPRESSION; GENE FUNCTION; GENE IDENTIFICATION; GENE MUTATION; GENE SEQUENCE; GENETIC ANALYSIS; GENETIC CODE; GENOME; ISOLATION PROCEDURE; NONHUMAN; PHENOTYPE; PPGPP SYNTHETASE GENE; PRIORITY JOURNAL; SPOT GENE; VIBRIO CHOLERAE; VIRUS GENE; VIRUS STRAIN;

AMINO ACID SEQUENCE; BACTERIAL PROTEINS; DNA, BACTERIAL; ESCHERICHIA COLI; GENE EXPRESSION REGULATION, BACTERIAL; GENES, BACTERIAL; GUANOSINE PENTAPHOSPHATE; LIGASES; MOLECULAR SEQUENCE DATA; PHENOTYPE; POINT MUTATION; PYROPHOSPHATASES; SEQUENCE ANALYSIS, DNA; VIBRIO CHOLERAE;

ESCHERICHIA COLI; NEGIBACTERIA; VIBRIO CHOLERAE;

EID: 64149130399     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2009.06653.x     Document Type: Article

References (44)

1. Aravind, L. Koonin, E.V. (1998) The HD domain defines a new superfamily of metal-dependent phosphohydrolases. Trends Biochem Sci 23 : 469 472.
2. Ausubel, F.M., Brent, R., Kingston, R.E., Moore, D.D., Seidman, J.G., Smith, J.A. Struhl, K. (1989) Current Protocols in Molecular Biology. New York : John Wiley and Sons.
3. Battesti, A. Bouveret, E. (2006) Acyl carrier protein/SpoT interaction, the switch linking SpoT-dependent stress response to fatty acid metabolism. Mol Microbiol 62 : 1048 1063.
4. van der Biezen, E.A., Sun, J., Coleman, M.J., Bibb, M.J. Jones, J.D. (2000) Arabidopsis RelA/SpoT homologs implicate (p)ppGpp in plant signaling. Proc Natl Acad Sci USA 97 : 747 752.
5. Cashel, M., Gentry, D.R., Hernandes, V.J. Vinella, D. (1996) The stringent response. In Escherichia coli and Salmonella typhimurium: Cellular and Molecular Biology. Neidhardt, F.C. (ed.). Washington, DC : American Society for Microbiology, pp. 1458 1496.
6. Choy, H.E. (2000) The study of guanosine 5′-diphosphate 3′-diphosphate-mediated transcription regulation in vitro using a coupled transcription-translation system. J Biol Chem 275 : 6783 6789.
7. Das, B. Bhadra, R.K. (2008) Molecular characterization of Vibrio choleraeΔrelAΔspoT double mutants. Arch Microbiol 189 : 227 238.
8. Gentry, D.R. Cashel, M. (1996) Mutational analysis of the Escherichia coli spoT gene identifies distinct but overlapping regions involved in ppGpp synthesis and degradation. Mol Microbiol 19 : 1373 1384.
9. Gropp, M., Strausz, Y., Gross, M. Glasser, G. (2001) Regulation of Escherichia coli RelA requires oligomerization of the C-terminal domain. J Bacteriol 183 : 570 579.
10. Guzman, L.M., Belin, D., Carson, M.J. Beckwith, J. (1995) Tight regulation, modulation and high-level expression by vectors containing the arabinose PBAD promoter. J Bacteriol 177 : 4121 4130.
11. Haralalka, S., Nandi, S. Bhadra, R.K. (2003) Mutation in the relA gene of Vibrio cholerae affects in vitro and in vivo expression of virulence factors. J Bacteriol 185 : 4672 4682.
12. Haseltine, W.A. Block, R. (1973) Synthesis of guanosine tetra- and pentaphosphate requires the presence of a codon-specific, uncharged transfer ribonucleic acid in the acceptor site of ribosomes. Proc Natl Acad Sci USA 70 : 1564 1568.
13. Heidelberg, J.F., Eisen, J.A., Nelson, W.C., Clayton, R.A., Gwinn, M.L., Dodson, R.J., et al. (2000) DNA sequence of both chromosomes of the cholera pathogen Vibrio cholerae. Nature 406 : 477 483.
14. Hogg, T., Mechold, U., Malke, H., Cashel, M. Hilgenfeld, R. (2004) Conformational antagonism between opposing active sites in a bifunctional RelA/SpoT homolog modulates (p)ppGpp metabolism during the stringent response. Cell 117 : 57 68.
15. Jishage, M., Kvint, K., Shingler, V. Nyström, T. (2002) Regulation of sigma factor competition by the alarmone ppGpp. Genes Dev 16 : 1260 1270.
16. Kasai, K., Usami, S., Yamada, T., Endo, Y., Ochi, K. Tozawa, Y.A. (2002) RelA-SpoT homolog (Cr-RSH) identified in Chlamydomonas reinhardtii generates stringent factor in vivo and localizes to chloroplasts in vitro. Nucleic Acids Res 30 : 4985 4992.
17. Lemos, J.A., Lin, V.K., Nascimento, M.M., Abranches, J. Burne, R.A. (2007) Three gene products govern (p)ppGpp production by Streptococcus mutans. Mol Microbiol 65 : 1568 1581.
18. Magnusson, L.U., Gummesson, B., Joksimoviæ, P., Farewell, A. Nyström, T. (2007) Identical, independent, and opposing roles of ppGpp and DksA in Escherichia coli. J Bacteriol 189 : 5193 5202.
19. Mechold, U., Cashel, M., Steiner, K., Gentry, D. Malke, H. (1996) Functional analysis of a relA/spoT gene homolog from Streptococcus equisimilis. J Bacteriol 178 : 1401 1411.
20. Seq the Rel/Spo enzyme from Streptococcus equisimilis. J Bacteriol 184 : 2878 2888.
21. Metzger, S., Schreiber, G., Aizenman, E., Cashel, M. Glaser, G. (1989) Characterization of the relA1 mutation and a comparison of relA1 with new relA null alleles in Escherichia coli. J Biol Chem 264 : 21146 21152.
22. Milon, P., Tischenko, E., Tomsic, J., Caserta, E., Folkers, G., La Teana, A., et al. (2006) The nucleotide-binding site of bacterial translation initiation factor 2 (IF2) as a metabolic sensor. Proc Natl Acad Sci USA 103 : 13962 13967.
23. Mittenhuber, G. (2001) Comparative genomics and evolution of genes encoding bacterial (p)ppGpp synthetases/hydrolases (the Rel, RelA and SpoT proteins). J Mol Microbiol Biotechnol 3 : 585 600.
24. Mizusawa, K., Masuda, S. Ohta, H. (2008) Expression profiling of four RelA/SpoT-like proteins, homologues of bacterial stringent factors. Arabidopsis thaliana. Planta 228 : 553 562.
25. Moche, M., Schneider, G., Edwards, P., Dehesh, K. Lindqvist, Y. (1999) Structure of the complex between the antibiotic cerulenin and its target, beta-ketoacyl-acyl carrier protein synthase. J Biol Chem 274 : 6031 6034.
26. Nanamiya, H., Kasai, K., Nozawa, A., Yun, C.S., Narisawa, T., Murakami, K., et al. (2008) Identification and functional analysis of novel (p)ppGpp synthetase genes in Bacillus subtilis. Mol Microbiol 67 : 291 304.
27. Omura, S. (1981) Cerulenin. Methods Enzymol 72 : 520 532.
28. Potrykus, K. Cashel, M. (2008) (p)ppGpp: still magical? Annu Rev Microbiol 62 : 35 51.
29. Rudd, K.E., Bochner, B.R., Cashel, M. Roth, J.R. (1985) Mutation in the spoT gene of Salmonella typhimurium: effects on his operon expression. J Bacteriol 163 : 534 542.
30. Sajish, M., Tiwari, D., Rananaware, D., Nandicoori, V.K. Prakash, B. (2007) A charge reversal differentiates (p)ppGpp synthesis by monofunctional and bifunctional Rel proteins. J Biol Chem 282 : 34977 34983.
31. Schreiber, G., Metzger, S., Aizenman, E., Roza, S., Cashel, M. Glaser, G. (1991) Overexpression of the relA gene in Escherichia coli. J Biol Chem 266 : 3760 3767.
32. Seyfzadeh, M., Keener, J. Nomura, M. (1993) spoT-dependent accumulation of guanosine tetraphosphate in response to fatty acid starvation in Escherichia coli. Proc Natl Acad Sci USA 90 : 11004 11008.
33. Shah, S., Das, B. Bhadra, R.K. (2008) Functional analysis of the essential GTP-binding-protein-coding gene cgtA of Vibrio cholerae. J Bacteriol 190 : 4764 4771.
34. Silva, A.J. Benitez, J.A. (2006) A Vibrio cholerae relaxed (relA) mutant expresses major virulence factors, exhibits biofilm formation and motility, and colonizes the suckling mouse intestine. J Bacteriol 188 : 794 800.
35. Skorupski, K. Taylor, R.K. (1996) Positive selection vectors for allelic exchange. Gene 169 : 47 52.
36. Stephens, J.C., Artz, S.W. Ames, B.N. (1975) Guanosine 5′-diphosphate 3′-diphosphate (ppGpp): positive effector for histidine operon transcription and general signal for amino-acid deficiency. Proc Natl Acad Sci USA 72 : 4389 4393.
37. Svitil, A.L., Cashel, M. Zyskind, J.W. (1993) Guanosine tetraphosphate inhibits protein synthesis in vivo. A possible protective mechanism for starvation stress in Escherichia coli. J Biol Chem 268 : 2307 2311.
38. Takahashi, K., Kasai, K. Ochi, K. (2004) Identification of the bacterial alarmone guanosine 5′-diphosphate 3′-diphosphate (ppGpp) in plants. Proc Natl Acad Sci USA 101 : 4320 4324.
39. Tozawa, Y., Nozawa, A., Kanno, T., Narisawa, T., Masuda, S., Kasai, K. Nanamiya, H. (2007) Calcium-activated (p)ppGpp synthetase in chloroplasts of land plants. J Biol Chem 282 : 35536 35545.
40. - mutants. Mol Gen Genet 165 : 21 30.
41. Vinella, D., Albrecht, C., Cashel, M. Ari, R. (2005) Iron limitation induces SpoT-dependent accumulation of ppGpp in Escherichia coli. Mol Microbiol 56 : 958 970.
42. Wang, J.D., Sanders, G.M. Grossman, A.D. (2007) Nutritional control of elongation of DNA replication by (p)ppGpp. Cell 128 : 865 875.
43. Wendrich, T.M., Blaha, G., Wilson, D.N., Marahiel, M.A. Nierhaus, K.H. (2002) Dissection of the mechanism for the stringent factor RelA. Mol Cell 10 : 779 788.
44. Xiao, H., Kalman, M., Ikehara, K., Zamel, S., Glaser, G. Cashel, M. (1991) Residual guanosine 3′, 5′-bispyrophosphate synthetic activity of relA null mutants can be eliminated by spoT null mutations. J Biol Chem 266 : 5980 5990.