Phosphatases modulate the bistable sporulation gene expression pattern in Bacillus subtilis

Molecular Microbiology

Volumn 56, Issue 6, 2005, Pages 1481-1494

  Veening, Jan Willem ^a   Hamoen, Leendert W ^a,b   Kuipers, Oscar P ^a  

^a UNIVERSITY OF GRONINGEN   (Netherlands)

^b UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

GREEN FLUORESCENT PROTEIN; PHOSPHATASE; RAP PHOSPHATASE; RNA POLYMERASE; SIGMA FACTOR; SPOOA PROTEIN; SPOOE PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; BACILLUS SUBTILIS; BACTERIUM CULTURE; FLOW CYTOMETRY; FLUORESCENCE MICROSCOPY; GENE DELETION; GENE EXPRESSION; NONHUMAN; OPERON; PHENOTYPIC VARIATION; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROMOTER REGION; SPOROGENESIS; STARVATION; WESTERN BLOTTING;

BACILLUS SUBTILIS; BACTERIAL PROTEINS; CULTURE MEDIA; FLOW CYTOMETRY; GENE EXPRESSION REGULATION, BACTERIAL; PHOSPHOPROTEIN PHOSPHATASE; PHOSPHORIC MONOESTER HYDROLASES; PROMOTER REGIONS (GENETICS); SPORES, BACTERIAL; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC;

BACILLUS SUBTILIS; BACTERIA (MICROORGANISMS); BACTERIUM SUBTILIS; POSIBACTERIA;

EID: 20344374152     PISSN: 0950382X     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2005.04659.x     Document Type: Article

References (61)

1. Balaban, N.Q., Merrin, J., Chait, R., Kowalik, L., and Leibler, S. (2004) Bacterial persistence as a phenotypic switch. Science 305: 1622-1625.
2. Becskei, A., Seraphin, B., and Serrano, L. (2001) Positive feedback in eukaryotic gene networks: cell differentiation by graded to binary response conversion. EMBO J 20: 2528-2535.
3. Bird, T., Burbulys, D., Wu, J.J., Strauch, M.A., Hoch, J.A., and Spiegelman, G.B. (1992) The effect of supercoiling on the in vitro transcription of the spoIIA operon from Bacillus subtilis. Biochimie 74: 627-634.
4. Blake, W.J., Kaern, M., Cantor, C.R., and Collins, J.J. (2003) Noise in eukaryotic gene expression. Nature 422: 633-637.
5. Burbulys, D., Trach, K.A., and Hoch, A. (1991) Initiation of sporulation in B. subtilis is controlled by a multicomponent phosphorelay. Cell 64: 545-552.
6. Cahn, F.H., and Fox, M.S. (1968) Fractionation of transformable bacteria from competent cultures of Bacillus subtilis on renografin gradients. J Bacteriol 95: 867-875.
7. Chung, J.D., Stephanopoulos, G., Ireton, K., and Grossman, A.D. (1994) Gene expression in single cells of Bacillus subtilis: evidence that a threshold mechanism controls the initiation of sporulation. J Bacteriol 176: 1977-1984.
8. Dawes, I.W., and Thornley, J.H. (1970) Sporulation in Bacillus subtilis. Theoretical and experimental studies in continuous culture systems. J Gen Microbiol 62: 49-66.
9. Elowitz, M.B., Levine, A.J., Siggia, E.D., and Swain, P.S. (2002) Stochastic gene expression in a single cell. Science 297: 1183-1186.
10. Ferrell, J.E., Jr. (2002) Self-perpetuating states in signal transduction: positive feedback, double-negative feedback and bistability. Curr Opin Cell Biol 14: 140-148.
11. Fujita, M., and Losick, R. (2003) The master regulator for entry into sporulation in Bacillus subtilis becomes a cell-specific transcription factor after asymmetric division. Genes Dev 17: 1166-1174.
12. Fujita, M., and Sadaie, Y. (1998) Feedback loops involving Spo0A and AbrB in in vitro transcription of the genes involved in the initiation of sporulation in Bacillus subtilis. J Biochem (Tokyo) 124: 98-104.
13. Fujita, M., Gonzalez-Pastor, J.E., and Losick, R. (2005) High-and low-threshold genes in the Spo0A regulon of Bacillus subtilis. J Bacteriol 187: 1357-1368.
14. Gardner, T.S., Cantor, C.R., and Collins, J.J. (2000) Construction of a genetic toggle switch in Escherichia coli. Nature 403: 339-342.
15. Gonzalez-Pastor, J.E., Hobbs, E.C., and Losick, R. (2003) Cannibalism by sporulating bacteria. Science 301: 510-513.
16. Grossman, A.D. (1995) Genetic networks controlling the initiation of sporulation and the development of genetic competence in Bacillus subtilis. Annu Rev Genet 29: 477-508.
17. Hadden, C., and Nester, E.W. (1968) Purification of competent cells in the Bacillus subtilis transformation system. J Bacteriol 95: 876-885.
18. Hahn, J., Kong, L., and Dubnau, D. (1994) The regulation of competence transcription factor synthesis constitutes a critical control point in the regulation of competence in Bacillus subtilis. J Bacteriol 176: 5753-5761.
19. Hahn, J., Roggiani, M., and Dubnau, D. (1995) The major role of Spo0A in genetic competence is to downregulate abrB, an essential competence gene. J Bacteriol 177: 3601-3605.
20. Hasty, J., Pradines, J., Dolnik, M., and Collins, J.J. (2000) Noise-based switches and amplifiers for gene expression. Proc Natl Acad Sci USA 97: 2075-2080.
21. Hoch, J.A. (1991) Spo0 genes, the phosphorelay, and the initiation of sporulation. In Bacillus Subtilis and Other Gram-Positive Bacteria: Biochemistry, Physiology, and Molecular Genetics. Sonenshein, A.L., Hoch, J.A., and Losick, R. (eds). Washington, DC: American Society for Microbiology, pp. 747-755.
22. Hofer, T., Nathansen, H., Lohning, M., Radbruch, A., and Heinrich, R. (2002) GATA-3 transcriptional imprinting in Th2 lymphocytes: a mathematical model. Proc Natl Acad Sci USA 99: 9364-9368.
23. Hosoya, S., Asai, K., Ogasawara, N., Takeuchi, M., and Sato, T. (2002) Mutation in yaaT leads to significant inhibition of phosphorelay during sporulation in Bacillus subtilis. J Bacteriol 184: 5545-5553.
24. Ireton, K., Rudner, D.Z., Siranosian, K.J., and Grossman, A.D. (1993) Integration of multiple developmental signals in Bacillus subtilis through the Spo0A transcription factor. Genes Dev 7: 283-294.
25. Isaacs, F.J., Hasty, J., Cantor, C.R., and Collins, J.J. (2003) Prediction and measurement of an autoregulatory genetic module. Proc Natl Acad Sci USA 100: 7714-7719.
26. Koetje, E.J., Hajdo-Milasinovic, A., Kiewiet, R., Bron, S., and Tjalsma, H. (2003) A plasmid-borne Rap-Phr system of Bacillus subtilis can mediate cell-density controlled production of extracellular proteases. Microbiology 149: 19-28.
27. Kunst, F., Ogasawara, N., Moszer, I., Albertini, A.M., Alloni, G., Azevedo, V., et al. (1997) The complete genome sequence of the Gram-positive bacterium Bacillus subtilis. Nature 390: 249-256.
28. Lazazzera, B.A., Palmer, T., Quisel, J., and Grossman, A.D. (1999) Cell density control of gene expression and development in Bacillus subtilis. In Cell-cell Signaling in Bacteria. Dunny, G.M., and Winans, S.C. (eds). Washington, DC: American Society for Microbiology, pp. 27-46.
29. Lewis, P.J., and Marston, A.L. (1999) GFP vectors for controlled expression and dual labelling of protein fusions in Bacillus subtilis. Gene 227: 101-110.
30. McAdams, H.H., and Arkin, A. (1997) Stochastic mechanisms in gene expression. Proc Natl Acad Sci USA 94: 814-819.
31. Maughan, H., and Nicholson, W.L. (2004) Stochastic processes influence stationary-phase decisions in Bacillus subtilis. J Bacteriol 186: 2212-2214.
32. Meijer, W.J., Wisman, G.B., Terpstra, P., Thorsted, P.B., Thomas, C.M., Holsappel, S., et al. (1998) Rolling-circle plasmids from Bacillus subtilis: complete nucleotide sequences and analyses of genes of pTA1015, pTA1040, pTA1050 and pTA1060, and comparisons with related plasmids from Gram-positive bacteria. FEMS Microbiol Rev 21: 337-368.
33. Molle, V., Fujita, M., Jensen, S.T., Eichenberger, P., Gonzalez-Pastor, J.E., Liu, J.S., and Losick, R. (2003) The Spo0A regulon of Bacillus subtilis. Mol Microbiol 50: 1683-1701.
34. Mueller, J.P., and Sonenshein, A.L. (1992) Role of the Bacillus subtilis gsiA gene in regulation of early sporulation gene expression. J Bacteriol 174: 4374-4383.
35. Mueller, J.P., Bukusoglu, G., and Sonenshein, A.L. (1992) Transcriptional regulation of Bacillus subtilis glucose starvation-inducible genes: control of gsiA by the ComP-ComA signal transduction system. J Bacteriol 174: 4361-4373.
36. Nakano, M.M., Xia, L.A., and Zuber, P. (1991a) Transcription initiation region of the srfA operon, which is controlled by the comP-comA signal transduction system in Bacillus subtilis. J Bacteriol 173: 5487-5493.
37. Nakano, M.M., Magnuson, R., Myers, A., Curry, J., Grossman, A.D., and Zuber, P. (1991b) srfA is an operon required for surfactin production, competence development, and efficient sporulation in Bacillus subtilis. J Bacteriol 173: 1770-1778.
38. Ohlsen, K.L., Grimsley, J.K., and Hoch, J.A. (1994) Deactivation of the sporulation transcription factor Spo0A by the Spo0E protein phosphatase. Proc Natl Acad Sci USA 91: 1756-1760.
39. Ozbudak, E.M., Thattai, M., Kurtser, I., Grossman, A.D., and van Oudenaarden, A. (2002) Regulation of noise in the expression of a single gene. Nat Genet 31: 69-73.
40. Parker, G.F., Daniel, R.A., and Errington, J. (1996) Timing and genetic regulation of commitment to sporulation in Bacillus subtilis. Microbiology 142: 3445-3452.
41. Perego, M. (1999) Self-signaling by Phr peptides modulates Bacillus subtilis development. In Cell-cell Signaling in Bacteria. Dunny, G.M., and Winans, S.C. (eds). Washington, DC: American Society for Microbiology, pp. 243-258.
42. Perego, M., and Hoch, J.A. (1991) Negative regulation of Bacillus subtilis sporulation by the spo0E gene product. J Bacteriol 173: 2514-2520.
43. Perego, M., and Hoch, J.A. (1996) Cell-cell communication regulates the effects of protein aspartate phosphatases on the phosphorelay controlling development in Bacillus subtilis. Proc Natl Acad Sci USA 93: 1549-1553.
44. Perego, M., and Hoch, J.A. (2002) Two-component systems, phosphorelays, and regulation of their activities by phosphatases. In Bacillus subtilis and its Closest Relatives: from Genes to Cells. Sonenshein, A.L., Hoch, J.A., and Losick, R. (eds). Washington, DC: American Society for Microbiology Press, pp. 473-481.
45. Predich, M., Nair, G., and Smith, I. (1992) Bacillus subtilis early sporulation genes kinA spo0F, and spo0A are transcribed by the RNA polymerase containing sigma H. J Bacteriol 174: 2771-2778.
46. Rao, C.V., Wolf, D.M., and Arkin, A.P. (2002) Control, exploitation and tolerance of intracellular noise. Nature 420: 231-237.
47. Raser, J.M., and O'Shea, E.K. (2004) Control of stochasticity in eukaryotic gene expression. Science 304:1811-1814.
48. Robertson, J.B., Gocht, M., Marahiel, M.A., and Zuber, P. (1989) AbrB, a regulator of gene expression in Bacillus, interacts with the transcription initiation regions of a sporulation gene and an antibiotic biosynthesis gene. Proc Natl Acad Sci USA 86: 8457-8461.
49. Sambrook, J., Fritsch, E.F., and Maniatis, T. (1989) Molecular Cloning: a Laboratory Manual Cold Spring Harbor. New York, NY: Cold Spring Harbor Laboratory Press.
50. Smits, W.K., Eschevins, C.C., Susanna, K.A., Bron, S., Kuipers, O.P., and Hamoen, L.W. (2005) Stripping Bacillus: Comk auto-stimulation is responsible for the bistable response in competence development. Mol Microbiol 56: 604-614.
51. Sonenshein, A.L. (2000) Control of sporulation initiation in Bacillus subtilis. Curr Opin Microbiol 3: 561-566.
52. Steinmetz, M., and Richter, R. (1994) Plasmids designed to alter the antibiotic resistance expressed by insertion mutations in Bacillus subtilis, through in vivo recombination. Gene 142: 79-83.
53. Strauch, M.A. (1995) Delineation of AbrB-binding sites on the Bacillus subtilis spo0H, kinB, ftsAZ, and pbpE promoters and use of a derived homology to identify a previously unsuspected binding site in the bsuB1 methylase promoter. J Bacteriol 177: 6999-7002.
54. Strauch, M.A., Spiegelman, G.B., Perego, M., Johnson, W.C., Burbulys, D., and Hoch, J.A. (1989) The transition state transcription regulator abrB of Bacillus subtilis is a DNA binding protein. EMBO J 8: 1615-1621.
55. Strauch, M.A., Trach, K.A., Day, J., and Hoch, J.A. (1992) Spo0A activates and represses its own synthesis by binding at its dual promoters. Biochimie 74: 619-626.
56. Strauch, M.A., Wu, J.J., Jonas, R.H., and Hoch, J.A. (1993) A positive feedback loop controls transcription of the spo0F gene, a component of the sporulation phosphorelay in Bacillus subtilis. Mol Microbiol 7: 967-974.
57. Tjalsma, H., Koetje, E.J., Kiewiet, R., Kuipers, O.P., Kolkman, M., van der Laan, J., et al. (2004) Engineering of quorum-sensing systems for improved production of alkaline protease by Bacillus subtilis. J Appl Microbiol 96: 569-578.
58. Veening, J.W., Smits, W.K., Hamoen, L.W., Jongbloed, J.D., and Kuipers, O.P. (2004) Visualization of Differential Gene Expression by Improved Cyan Fluorescent Protein and Yellow Fluorescent Protein Production in Bacillus subtilis. Appl Environ Microbiol 70: 6809-6815.
59. Weinrauch, Y., Guillen, N., and Dubnau, D.A. (1989) Sequence and transcription mapping of Bacillus subtilis competence genes comB and comA, one of which is related to a family of bacterial regulatory determinants. J Bacteriol 171: 5362-5375.
60. Wertman, K.F., Wyman, A.R., and Botstein, D. (1986) Host/ vector interactions which affect the viability of recombinant phage lambda clones. Gene 49: 253-262.
61. Xu, K., and Strauch, M.A. (1996) Identification, sequence, and expression of the gene encoding gamma-glutamyl-transpeptidase in Bacillus subtilis. J Bacteriol 178: 4319-4322.