Differential responses of Bacillus subtilis rRNA promoters to nutritional stress

Journal of Bacteriology

Volumn 193, Issue 3, 2011, Pages 723-733

  Samarrai, Walied ^b   Liu, David X ^c   White, Ann Marie ^d   Studamire, Barbara ^e   Edelstein, Jacob ^a   Srivastava, Anita ^a   Widom, Russell L ^f   Rudner, Rivka ^a  

^a CITY UNIVERSITY OF NEW YORK   (United States)

^b NEW YORK CITY COLLEGE OF TECHNOLOGY   (United States)

^c PENN STATE COLLEGE OF MEDICINE   (United States)

^d Deerfield Academy   (United States)

^e CITY UNIVERSITY OF NEW YORK   (United States)

^f Occhiuti Rohlicek and Tsao   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL RNA; MESSENGER RNA; RIBOSOME RNA;

ARTICLE; BACILLUS SUBTILIS; BACTERIAL GROWTH; BACTERIUM CULTURE; CARBON SOURCE; GENE LOCUS; NONHUMAN; NUTRITION; PRIORITY JOURNAL; PROMOTER REGION; RNA ANALYSIS; RNA SYNTHESIS; STRESS;

ARTIFICIAL GENE FUSION; BACILLUS SUBTILIS; BETA-GALACTOSIDASE; GENE EXPRESSION REGULATION, BACTERIAL; GENES, REPORTER; GUANOSINE TETRAPHOSPHATE; PROMOTER REGIONS, GENETIC; RNA, RIBOSOMAL; STRESS, PHYSIOLOGICAL; TRANSCRIPTION, GENETIC;

BACILLUS SUBTILIS;

EID: 78751538121     PISSN: 00219193     EISSN: 10985530     Source Type: Journal    
DOI: 10.1128/JB.00708-10     Document Type: Article

References (59)

1. Adyha, S., and M. Gottesman. 1982. Promoter occlusion: transcription through a promoter may inhibit its activity. Cell 29:939-944.
2. a.Afflerbach, H., O. Schroder, and R. Wagner. 1998. Effects of the Escherichia coli DNA-binding protein H-NS on rRNA synthesis in vivo. Mol. Microbiol. 28:641-653.
3. Anagnostopoulos, C., P. J. Piggot, and James A. Hoch. 1993. The genetic map of Bacillus subtilis, p. 425-462. In A. L. Sonenshein, J. A. Hoch, and R. Losick (ed.), Bacillus subtilis and its closest relatives: from genes to cells. ASM Press, Washington, DC.
4. Anagnostopoulos, C., and J. Spizizen 1961. Requirements for transformation in Bacillus subtilis. J. Bacteriol. 81: 741-746.
5. Antoniewski, C., B. Savelli, and P. Stragier. 1990. The spoIIJ gene, which regulates early developmental steps in Bacillus subtilis, belongs to a class of environmentally responsive genes. J. Bacteriol. 172:86-93.
6. Barker, M. M., and R. L. Gourse. 2001. Regulation of rRNA transcription correlates with nucleoside triphosphate sensing. J. Bacteriol. 183:6315-6323.
7. Bechhofer, D. H., and K. H. Zen. 1989. Mechanism of erythromycin-induced ermC mRNA stability in Bacillus subtilis. J. Bacteriol. 171:5803-5811.
8. Cashel, M., D. R. Gentry, V. J. Hernandez, and D. Vinella. 1996. The stringent response, p. 1458-1496. In F. C. Neidhardt et al. (ed.), Escherichia coli and Salmonella: cellular and molecular biology. ASM Press: Washington, DC.
9. Condon, C., C. Squires, and C. L. Squires. 1995. Control of rRNA transcription in Escherichia coli. Microbiol. Rev. 59:623-645.
10. Davies, K. M., and P. J. Lewis. 2003. Localization of rRNA synthesis in Bacillus subtilis: characterization of loci involved in transcription focus formation. J. Bacteriol. 185:2346-2353.
11. Deneer, H. G., and G. B. Spiegelman. 1987. Bacillus subtilis rRNA promoters are growth rate regulated in Escherichia coli. J. Bacteriol. 169:995-1002.
12. Fukushima, T., S. Ishikawa, H. Yamamoto, N. Ogasawara, and J. Sekiguchi. 2003. Transcriptional, functional and cytochemical analyses of the veg gene in Bacillus subtilis. J. Biochem. 133:475-483.
13. Gaal, T., M. S. Bartlett, W. Ross, C. L. Turnbough, Jr., and R. L. Gourse. 1997. Transcription regulation by initiating NTP concentration: rRNA synthesis in bacteria. Science 278:2092-2097.
14. Gafny, R., S. Cohen, N. Nachaliel, and G. Glaser. 1994. Isolated P2 rRNA promoters of Escherichia coli are strong promoters that are subject to stringent control. J. Mol. Biol. 243:152-156.
15. Gallant, J., G. Margason, and B. Finch. 1972. On the turnover of ppGpp in Escherichia coli. J. Biol. Chem. 247:6055-6058.
16. Gourse, R. L., T. Gaal, M. S. Bartlett, J. A. Appleman, and W. Ross. 1996. rRNA transcription and growth rate-dependent regulation of ribosome synthesis in Escherichia coli. Annu. Rev. Microbiol. 50:645-677.
17. Green, C. J., G. C. Stewart, M. A. Hollis, B. S. Vold, and K. F. Bott. 1985. Nucleotide sequence of the Bacillus subtilis ribosomal RNA operon rrnB. Gene 37:261-266.
18. Green, C. J., and B. S. Vold. 1993. tRNA, tRNA processing, and aminoacyltRNA sythetases, p. 683-698. In A. L. Sonenshein, J. A. Hoch, and R. Losick (ed.), Bacillus subtilis and other gram-positive bacteria: biochemistry, physiology, and molecular genetics. American Society for Microbiology, Washington, DC.
19. Gropp, M., E. Eizenman, G. Glaser, W. Samarrai, and R. Rudner. 1994. A relAS suppressor mutant allele of Bacillus subtilis which maps to relA and responds only to carbon limitation. Gene 140:91-96.
20. Hambraeus, G., C. von Wachenfeldt, and L. Hederstedt. 2003. Genome-wide survey of mRNA half-lives in Bacillus subtilis identifies extremely stable mRNAs. Mol. Genet. Genomics 269:706-714.
21. Henkin, T. M. 2002. Ribosomes, protein synthesis factors, and tRNA synthetases, p. 313-322. In A. L. Sonenshein, J. A. Hoch, and R. Losick (ed.), Bacillus subtilis and its closest relatives: from genes to cells. ASM Press, Washington, DC.
22. Hilton, J., P. C. Kearney, and B. N. Ames. 1965. Mode of action of the herbicide 8-amino 1,2,4 triazole: inhibition of an enzyme of histidine biosynthesis. Arch. Biochem. Biophys. 112:544-547.
23. Hirata, H., T. Fukazawa, S. Negro, and H. Okada. 1986. Structure of β-galactosidase gene of Bacillus stearothermophilus. J. Bacteriol. 166:722-727.
24. Hirvonen, C. A., et al. 2001. Contributions of UP elements and the transcription factor FIS to expression from the seven rrn P1 promoters in Escherichia coli. J. Bacteriol. 183:6305-6314.
25. Horinouchi, S., and B. Weisblum. 1982. Nucleotide sequence and functional map of pE194, a plasmid that specifies inducible resistance to macrolide, lincosamide, and streptogramin type B antibiotics. J. Bacteriol. 150:804-814.
26. b.Horinouchi, S., and B. Weisblum. 1982. Nucleotide sequence and functional map of pC194, a plasmid that specifies inducible chloramphenicol resistance. J. Bacteriol. 150:815-825.
27. Jarvis, E. D., et al. 1988. Chromosomal organization of rRNA operons in Bacillus subtilis. Genetics 120:625-635.
28. Kessler, D. P., and H. V. Rickenberg. 1963. The competitive inhibition of alpha-methylglucoside uptake in Escherichia coli. Biochem. Biophys. Res. Commun. 10:482-487.
29. a.Koga, K., et al. 2006. Construction of Bacillus subtilis strains carrying the transcriptional bgaB fusion with the promoter region of each rrn operon and their differential transcription during spore development. J. Gen. Appl. Microbiol. 52:119-124.
30. Krásny, L., and R. L. Gourse. 2004. An alternative strategy for bacterial ribosome synthesis: Bacillus subtilis rRNA transcription regulation. EMBO J. 23:4473-4483.
31. LaFauci, G., R. L. Widom, R. L. Eisner, E. D. Jarvis, and R. Rudner. 1986. Mapping of rRNA genes with integrable plasmids in Bacillus subtilis. J. Bacteriol. 165:204-214.
32. Lin, S., and I. Zabin. 1972. Beta-galactosidase. Rates of synthesis and degradation of incomplete chains. J. Biol. Chem. 247:2205-2211.
33. Liu, D. X. 1998. Differential regulation of the P1 and P2 promoters of ribosomal RNA operons in Bacillus subtilis. Ph.D. thesis. Hunter College of the City University of New York, New York, NY.
34. Margulies, L., V. Remeza, and R. Rudner. 1970. Asymmetric template function of microbial deoxyribonucleic acids: transcription of ribosomal and soluble ribonucleic acids. J. Bacteriol. 103:560-568.
35. Miller, J. H. 1972. Experiments in molecular genetics, p. 352-355. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY.
36. Murray, H. D., D. A. Schneider, and R. L. Gourse. 2003. Control of rRNA expression by small molecules is dynamic and nonredundant. Mol. Cell 12:125-134.
37. Murray, H. D., and R. L. Gourse. 2004. Unique roles of the rrn P2 rRNA promoters in Escherichia coli. Mol. Microbiol. 52:1375-1387.
38. Nachaliel, N., J. Melnick, R. Gafny, and G. Glaser. 1989. Ribosome associated protein(s) specifically bind(s) to the upstream activator sequence of the E. coli rrnA P1 promoter. Nucleic Acids Res. 17:9811-9822.
39. Nishino, T., J. Gallant, P. Shalit, L. Palmer, and T. Wehr. 1979. Regulatory nucleotides involved in the Rel function of Bacillus subtilis. J. Bacteriol. 140:671-679.
40. Ogasawara, N., S. Moriya, and H. Yoshikawa. 1985. Structure and function of the region of the replication origin of the Bacillus subtilis chromosome. IV. Transcription of the oriC region and expression of DNA gyrase genes and other open reading frames. Nucleic Acids Res. 13:2267-2279.
41. Oishi, M. 1969. The transcribing strands of Bacillus subtilis DNA for ribosomal and transfer RNA. Proc. Nat. Acad. Sci. U. S. A. 54:483-491.
42. Okamoto, K., and B. S. Vold. 1992. Activity of ribosomal and tRNA promoters of Bacillus subtilis during sporulation. Biochimie. 74:613-618.
43. Ollington, J. F., and R. Losick. 1981. A cloned gene that is turned on at an intermediate stage of spore formation in Bacillus subtilis. J. Bacteriol. 147: 443-451.
44. Paul, B. J., W. Ross, T. Gaal, and R. L. Gourse. 2004. rRNA transcription in Escherichia coli. Annu. Rev. Genet. 38:749-770.
45. Price, V. L., and J. A. Gallant. 1982. A new relaxed mutant of Bacillus subtilis. J. Bacteriol. 149:635-641.
46. Rudd, K. E., B. R. Bochner, M. Cashel, and J. R. Roth. 1985. Mutations in the spoT gene of Salmonella typhimurium: effects on his operon expression. J. Bacteriol. 163:534-542.
47. Rudner, R., et al. 1993. Two tRNA gene clusters associated with rRNA operons rrnD and rrnE in Bacillus subtilis. J. Bacteriol. 175:503-519.
48. Rudner, R., A. Murray, and N. Huda. 1999. Is there a link between mutation rates and the stringent response in Bacillus subtilis? Ann. N. Y. Acad. Sci. 870:418-422.
49. Samarrai, W. 1996. Differential response of Bacillus subtilis ribosomal RNA operons to nutritional stress. Ph.D. thesis. Hunter College of The City University of New York, New York, NY.
50. Schneider, W. C. 1957. Determination of nucleic acids in tissues by pentose analysis. Methods Enzymol. 3:680-684.
51. Schreier, H. J., and A. L. Sonenshein. 1986. Altered regulation of the glnA gene in glutamine synthetase mutants of Bacillus subtilis. J. Bacteriol. 167: 35-43.
52. Shimotsu, H., and D. J. Henner. 1986. Construction of a single-copy integration vector and its use in analysis of regulation of the trp operon of Bacillus subtilis. Gene 43:85-94.
53. Smith, I., P. Paress, K. Cabane, and E. Dubnau. 1980. Genetics and physiology of the rel system of Bacillus subtilis. Mol. Gen. Genet. 178:271-279.
54. Tosa, T., and L. I. Pizer. 1971. Biochemical bases for the antimetabolite action of L-serine hydroxamate. J. Bacteriol. 106:972-982.
55. Weir, J., M. Predich, E. Dubnau, G. Nair, and I. Smith. 1991. Regulation of spo0H, a gene coding for the Bacillus subtilis sigma H factor. J. Bacteriol. 173:521-529.
56. Wellington, S. R., and G. B. Spiegelman. 1993. The kinetics of formation of complexes between Escherichia coli RNA polymerase and the rrnB P1 and P2 promoters of Bacillus subtilis. Effects of guanosine tetraphosphate on select steps of transcription initiation. J. Biol. Chem. 268:7205-7214.
57. Wendrich, T. M., and M. A. Marahiel. 1997. Cloning and characterization of a relA/spoT homologue from Bacillus subtilis. Mol. Microbiol. 26:65-79.
58. Widom, R. L. 1988. Ph.D. thesis. Hunter College of the City University of New York, New York, NY.
59. Widom, R. L., E. D. Jarvis, G. LaFauci, and R. Rudner. 1988. Instability of rRNA operons in Bacillus subtilis. J. Bacteriol. 170:605-610.