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Chapter 8 : Control of Cellular Development in Sporulating Bacteria by the Phosphorelay Two-Component Signal Transduction System

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Abstract:

The initiation of sporulation in bacteria is a cellular response to deteriorating conditions for growth and division. Sporulation may be coupled to the cell cycle to suppress division and permit the orderly synthesis of spore membrane structural components in concert with chromosome replication. The nature of the integration mechanism for all this information is now becoming apparent, and its various regulatory features are discussed in this chapter. The two-component paradigm is at the heart of the signal transduction system, regulating the initiation of sporulation in sporulating bacteria. This system, the phosphorelay, differs from other two-component signal transduction systems by the mechanism of phosphate flow and types of accessory proteins that control phosphate flow in the system. The ultimate goal of the phosphorelay is to produce Spo0A~P, the activated form of this transcription factor that recognizes the 7-bp 0A box in sporulation promoters. Separate phosphatase proteins may only be necessary when two-component signal transduction systems are sensitive to multiple signal input, such as in sporulation, which may exhaust the signal recognition capacity of the kinase. The initiation of sporulation has adopted the two-component signal transduction system and made some unique modifications to adapt it to process multiple signal inputs. As more and more controls are discovered that act on the phosphorelay, it becomes even more amazing that sporulation occurs at all.

Citation: Hoch J. 1995. Control of Cellular Development in Sporulating Bacteria by the Phosphorelay Two-Component Signal Transduction System, p 129-144. In Hoch J, Silhavy T (ed), Two-Component Signal Transduction. ASM Press, Washington, DC. doi: 10.1128/9781555818319.ch8

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Figures

Image of FIGURE 1
FIGURE 1

Phosphorelay signal transduction pathway of . The source of activated phosphate is either KinA or KinB, responding to signal A or signal B, respectively. The nature of the signals is unknown in both cases and, in the case of KinB, is thought to be transmitted through the cytoplasmic protein KapB. The flow of phosphate through the phosphorelay has the goal of producing Spo0A∼P, which is a transcription activator or repressor, recognizing the 7-bp sequence shown.

Citation: Hoch J. 1995. Control of Cellular Development in Sporulating Bacteria by the Phosphorelay Two-Component Signal Transduction System, p 129-144. In Hoch J, Silhavy T (ed), Two-Component Signal Transduction. ASM Press, Washington, DC. doi: 10.1128/9781555818319.ch8
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Image of FIGURE 2
FIGURE 2

Role of Spo0A∼P in transcription regulation of phosphorelay. The central goal of Spo0A∼P is depicted as either activation or repression of promoters. The small black boxes within the promoter show the location of 0A boxes. The + and - signs refer to the effect of Spo0A∼P on the 0A box. Promoters with more than one 0A box with opposite signs means Spo0A∼P is both an activator and a repressor of the promoter. Briefly, Spo0A∼P is an activator of σ promoters on the and genes and a repressor of the vegetative σ promoter on the gene and the gene. AbrB is a repressor of the transcription of the gene coding for σ. Spo0A∼P appears to play a role in the repression of the gene.

Citation: Hoch J. 1995. Control of Cellular Development in Sporulating Bacteria by the Phosphorelay Two-Component Signal Transduction System, p 129-144. In Hoch J, Silhavy T (ed), Two-Component Signal Transduction. ASM Press, Washington, DC. doi: 10.1128/9781555818319.ch8
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Image of FIGURE 3
FIGURE 3

Promoter switching at Spo0A promoter. The locations of the vegetative promoter P and the sporulation promoter P transcribed by σ and σ, respectively, are shown. The boxed nucleotides correspond to the 0A boxes, and the lines demarking both strands are the extent of coverage of each strand by the footprint analysis of Spo0A on this promoter. Note that the Spo0A boxes and positions of Spo0A binding occur between the P and the P promoters. Spo0A∼P is believed to bind preferentially at the top two 0A boxes, simultaneously accomplishing the repression of the P promoter and the activation of the P promoter. The Spo0A box located at about the -10 of the P promoter is believed to be a repression point where the P promoter is repressed when Spo0A∼P concentrations reach sufficiently high levels.

Citation: Hoch J. 1995. Control of Cellular Development in Sporulating Bacteria by the Phosphorelay Two-Component Signal Transduction System, p 129-144. In Hoch J, Silhavy T (ed), Two-Component Signal Transduction. ASM Press, Washington, DC. doi: 10.1128/9781555818319.ch8
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Image of FIGURE 4
FIGURE 4

Comparison of structural features of Spo0F and CheY. The structural features from the crystal structure of CheY of (A. ) and the structure of the Spo0F as determined by multidimensional nuclear magnetic resonance analyses (Feher, unpublished data) are presented. Wavy lines indicate regions of β-sheet, and black boxes indicate areas of β-helix.

Citation: Hoch J. 1995. Control of Cellular Development in Sporulating Bacteria by the Phosphorelay Two-Component Signal Transduction System, p 129-144. In Hoch J, Silhavy T (ed), Two-Component Signal Transduction. ASM Press, Washington, DC. doi: 10.1128/9781555818319.ch8
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Image of FIGURE 5
FIGURE 5

Kinase and phosphatase reactions on Spo0F. The kinases for sporulation are depicted as being activated by signal K, which either activates the autophosphorylation reaction of these kinases or converts the kinase to a phosphatase of Spo0F∼P. The actual mechanism of signal interpretation for either KinA or KinB on Spo0F has not been determined. Two phosphatases, RapA and RapB, are known to respond to different transcriptional activation signals, and presumably different effector molecules control their activity on Spo0F∼P. Sufficient Spo0F∼P for the production of Spo0A∼P only occurs in the absence of the activity of these (and perhaps other) phosphatases.

Citation: Hoch J. 1995. Control of Cellular Development in Sporulating Bacteria by the Phosphorelay Two-Component Signal Transduction System, p 129-144. In Hoch J, Silhavy T (ed), Two-Component Signal Transduction. ASM Press, Washington, DC. doi: 10.1128/9781555818319.ch8
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Image of FIGURE 6
FIGURE 6

Conversion of Spo0F∼P to Spo0A∼P. Spo0F∼P is a substrate for the Spo0B phosphotransferase, which transfers the phosphate group to Spo0A. Spo0A is depicted as inactive in the unphosphorylated state, and this probably occurs because the end-terminal 0A domain prevents access of the DNA binding domain to DNA. Phosphorylation of Spo0A causes a conformational change that exposes the DNA binding site, allowing this transcription factor to bind to 0A boxes in the promoters that it controls. The Spo0E protein is a phosphatase of activated Spo0A∼P and is thought to respond to some internal signal, signal E, of unknown nature.

Citation: Hoch J. 1995. Control of Cellular Development in Sporulating Bacteria by the Phosphorelay Two-Component Signal Transduction System, p 129-144. In Hoch J, Silhavy T (ed), Two-Component Signal Transduction. ASM Press, Washington, DC. doi: 10.1128/9781555818319.ch8
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Image of FIGURE 7
FIGURE 7

Relationship between SinR and Spo0A∼P. SinR is a repressor of sporulation capable of binding to the promoters of several protease genes, as well as the promoters for the stage II genes, , , and . SinI is an inhibitor of the repressive functions of SinR, and this protein is produced at the end of exponential growth to relieve repression of sporulation. Transcription of SinI is activated by the accumulation of Spo0A∼P and inhibited by both Hpr and AbrB transition state regulators. Spo0A∼P is also a required activator for the transcription of the genes.

Citation: Hoch J. 1995. Control of Cellular Development in Sporulating Bacteria by the Phosphorelay Two-Component Signal Transduction System, p 129-144. In Hoch J, Silhavy T (ed), Two-Component Signal Transduction. ASM Press, Washington, DC. doi: 10.1128/9781555818319.ch8
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References

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1. Antoniewski, C.,, B. Savelli,, and P. Stragier. 1990. The spoilJ gene, which regulates early developmental steps in Bacillus subtilis, belongs to a class of environmentally responsive genes. J. Bacteriol. 172: 86 93.
2. Bai, U.,, M. Lewandoski,, E. Dubnau,, and I. Smith. 1990. Temporal regulation of the Bacillus subtilis early sporulation gene spo0F. J. Bacteriol. 172: 5432 5439.
3. Brown, D. P.,, L. Ganova-Raeva,, B. D. Green,, S. R. Wilkinson,, M. Young,, and P. Youngman. 1994. Characterization of spo0A homologues in diverse Bacillus and Clostridium species identifies a probable DNA-binding domain. Mol. Microbiol. 14: 411 426.
4. Burbulys, D.,, K. A. Trach,, and J. A. Hoch. 1991. The initiation of sporulation in Bacillus subtilis is controlled by a multicomponent phosphorelay. Cell 64: 545 552.
5. Charbonneau, H.,, and N. K. Tonks. 1992. 1002 protein phosphatases? Annu. Rev. Cell Biol. 8: 463 493.
6. Chibazakura, T.,, F. Kawamura,, and H. Takahashi. 1991. Differential regulation of spo0A transcription in Bacillus subtilis: glucose represses promoter switching at the initiation of sporulation. J. Bacteriol. 173: 2625 2632.
7. Dartois, V.,, and J. A. Hoch. Unpublished data.
8. Dubnau, D. 1991. The regulation of genetic competence in Bacillus subtilis. Mol. Microbiol. 5: 11 18.
9. Feher, V. Unpublished data.
10. Gaur, N. K.,, K. Cabane,, and I. Smith. 1988. Structure and expression of the Bacillus subtilis sin operon. J. Bacteriol. 170: 1046 1053.
11. Gaur, N. K.,, E. Dubnau,, and I. Smith. 1986. Characterization of a cloned Bacillus subtilis gene that inhibits sporulation in multiple copies. J. Bacteriol. 168: 860 869.
12. Gaur, N. K.,, J. Oppenheim,, and I. Smith. 1991. The Bacillus subtilis sin gene, a regulator of alternate developmental processes, codes for a DNA-binding protein J. Bacteriol. 173: 678 686.
13. Grimsley, J. K.,, R. B. Tjalkens,, M. A. Strauch,, T. H. Bird,, G. B. Spiegelman,, Z. Hostomsky,, J. M. Whiteley,, and J. A. Hoch. 1994. Subunit composition and domain structure of the Spo0A sporulation transcription factor of Bacillus subtilis. J. Biol. Chem. 269: 16977 16982.
14. Grossman, A. D.,, and R. Losick. 1988. Extracellular control of spore formation in Bacillus subtilis. Proc. Natl. Acad. Sci. USA 85: 4369 4373.
15. Healy, J.,, J. Weir,, I. Smith,, and R. Losick. 1991. Post-transcriptional control of a sporulation regulatory gene encoding transcription factor sigma H in Bacillus subtilis. Mol. Microbiol. 5: 477 487.
16. Hoch, J. A. Unpublished data.
17. Hubbard, M. J.,, and P. Cohen. 1993. On target with a new mechanism for the regulation of protein phosphorylation. Trends Biochem. Sci. 18: 172 177.
18. Ireton, K.,, and A. D. Grossman. 1994. A developmental checkpoint couples the initiation of sporulation to DNA replication in Bacillus subtilis. EMBO J. 13: 1566 1573.
19. Ireton, K.,, D. Z. Rudner,, K. J. Siranosian,, and A. D. Grossman. 1993. Integration of multiple developmental signals in Bacillus subtilis through the Spo0A transcription factor. Genes Dev. 7: 283 294.
20. Kallio, P. T.,, J. E. Fagelson,, J. A. Hoch,, and M. A. Strauch. 1991. The transition state regulator Hpr of Bacillus subtilis is a DNA-binding protein. J. Biol. Chem. 266: 13411 13417.
21. Kenney, T. J.,, P. A. Kirchrnan,, and C. P. J. Moran. 1988. Gene encoding sigma E is transcribed from a sigma A-like promoter in Bacillus subtilis. J. Bacteriol. 170: 3058 3064.
22. Lewandoski, M.,, E. Dubnau,, and I. Smith. 1986. Transcriptional regulation of the spoOF gene of Bacillus subtilis. J. Bacteriol. 168: 870 877.
23. Lopez, J. M.,, A. Dromerick,, and E. Freese. 1981. Response of guanosine 5'-triphosphate concentration to nutritional changes and its significance for Bacillus subtilis sporulation. J. Bacteriol. 146: 605 613.
24. Magnuson, R.,, J. Solomon,, and A. D. Grossman. 1994. Biochemical and genetic characterization of a competence pheromone from B. subtilis. Cell 77: 207 216.
25. Mandelstam, J.,, and S. A. Higgs. 1974. Induction of sporulation during synchronized chromosome replication in Bacillus subtilis. J. Bacteriol. 120: 38 42.
26. Mandic-Mulec, I.,, N. Gaur,, U. Bai,, and I. Smith. 1992. Sin, a stage-specific repressor of cellular differentiation. J. Bacteriol. 174: 3561 3569.
27. Mauro, L. J.,, and J. E. Dixon. 1994. "Zip codes" direct intracellular protein tyrosine phosphatases to the correct cellular "address." Trends Biochem. Sci. 19: 151 155.
28. McCleary, W. R.,, J. B. Stock,, and A. J. Ninfa. 1993. Is acetyl phosphate a global signal in Escherichia coli? J. Bacteriol. 175: 2793 2798.
29. Mueller, J. P.,, G. Bukusoglu,, and A. L. Sonenshein. 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.
30. Mueller, J. P.,, and A. L. Sonenshein. 1992. Role of the Bacillus subtilis gsiA gene in regulation of early sporulation gene expression. J. Bacteriol. 174: 4374 4383.
31. Mutoh, N.,, and M. I. Simon. 1986. Nucleotide sequence corresponding to five chemotaxis genes in Escherichia coli. J. Bacteriol. 165: 161 166.
32. Ohlsen, K. L.,, J. K. Grimsley,, and J. A. Hoch. 1994. Deactivation of the sporulation transcription factor Spo0A by the Spo0E protein phosphatase. Proc. Natl. Acad. Sci. USA 91: 1756 1760.
33. Perego, M. Unpublished data.
34. Perego, M.,, S. P. Cole,, D. Burbulys,, K. Trach,, and J. A. Hoch. 1989. Characterization of the gene for a protein kinase which phosphorylates the sporulation- regulatory proteins Spo0A and Spo0F of Bacillus subtilis. J. Bacteriol. 171: 6187 6196.
35. Perego, M.,, C. Hanstein,, K. M. Welsh,, T. Djavakhishvili,, P. Glaser,, and J. A. Hoch. 1994. Multiple protein-aspartate phosphatases provide a mechanism for the integration of diverse signals in the control of development in B. subtilis. Cell 79: 1047 1055.
36. Perego, M.,, C. F. Higgins,, S. R. Pearce,, M. P. Gallagher,, and J. A. Hoch. 1991. The oligopeptide transport system of Bacillus subtilis plays a role in the initiation of sporulation. Mol. Microbiol. 5: 173 185.
37. Perego, M.,, and J. A. Hoch. 1987. Isolation and sequence of the spo0E gene: its role in initiation of sporulation in Bacillus subtilis. Mol. Microbiol. 1: 125 132.
38. Perego, M.,, and J. A. Hoch. 1988. Sequence analysis and regulation of the hpr locus, a regulatory gene for protease production and sporulation in Bacillus subtilis. J Bacteriol. 170: 2560 2567.
39. Perego, M.,, and J. A. Hoch. 1991. Negative regulation of Bacillus subtilis sporulation by the spo0E gene product. J. Bacteriol. 173: 2514 2520.
40. Perego, M.,, and J. A. Hoch. Unpublished data.
41. Porter, S. C.,, A. K. North,, A. B. Wedel,, and S. Kustu. 1993. Oligomerization of NTRC at the glnA enhancer is required for transcriptional activation. Genes Dev. 7: 2258 2273.
42. Predich, M.,, G. Nair,, and I. Smith. 1992. Bacillus subtilis early sporulation genes kinA, spo0F, and spo0A are transcribed by the RNA polymerase containing σ H J Bacteriol. 174: 2771 2778.
43. Roman, S. J.,, M. Meyers,, K. Volz,, and P. Matsumura. 1992. A chemotactic signaling surface on CheY defined by suppressors of flagellar switch mutations. J. Bacteriol. 174: 6247 6255.
44. Rudner, D. Z.,, J. R. Ladeaux,, K. Breton,, and A. D. Grossman. 1991. The spo0K locus of Bacillus subtilis is homologous to the oligopeptide permease locus and is required for sporulation and competence. J. Bacteriol. 173: 1388 1398.
45. Sanders, D. A.,, B. L. Gillece-Castro,, A. L. Burlingame,, and D. E. Koshland, Jr. 1992. Phosphorylation site of NtrC, a protein phosphatase whose covalent intermediate activates transcription. J. Bacteriol. 174: 5117 5122.
46. Satola, S. W.,, J. M. Baldus,, and C. P. Moran, Jr. 1992. Binding of Spo0A stimulates spoIIG promoter activity in Bacillus subtilis. J. Bacteriol. 174: 1448 1453.
47. Smith, I., 1993. Regulatory proteins that control late growth development, p. 785 800. In A. L. Sonensheinj,, A. Hoch,, and R. Losick (ed.), Bacillus subtilis and Other Gram-Positive Bacteria: Biochemistry, Physiology and Molecular Genetics. American Society for Microbiology, Washington, D.C.
48. Sockett, H.,, S. Yamaguchi,, M. Kihara,, V. M. Irikura,, and R. M. Macnab. 1992. Molecular analysis of the flagellar switch protein FliM of Salmonella typhimurium. J. Bacteriol. 174: 793 806.
49. Stock, A. M.,, J. M. Mottonen,, J. B. Stock,, and C. E. Schutt. 1989. Three-dimensional structure of CheY, the response regulator of bacterial chemotaxis. Nature (London) 337: 745 749.
50. Stock, J. B.,, A. J. Ninfa,, and A. M. Stock. 1989. Protein phosphorylation and regulation of adaptive response in bacteria. Microbiol. Rev. 53: 450 490.
51. Strauch, M. Personal communication.
52. Strauch, M.,, V. Webb,, G. Spiegelman,, and J. A. Hoch. 1990. The Spo0A protein of Bacillus subtilis is a repressor of the abrB gene. Proc. Natl. Acad. Sci. USA 87: 1801 1805.
53. Strauch, M. A.,, and J. A. Hoch. 1992. Transition state regulators: sentinels of Bacillus subtilis post-exponential gene expression. Mol. Microbiol. 7: 337 342.
54. Strauch, M. A.,, K. A. Trach,, J. Day,, and J. A. Hoch. 1992a. Spo0A activates and represses its own synthesis by binding at its dual promoters. Biochimie 74: 619 626.
55. Strauch, M. A.,, J.-J. Wu,, R. H. Jonas,, and J. A. Hoch. 1992b. A positive feedback loop controls transcription of the spo0F gene, a component of the sporulation phosphorelay in Bacillus subtilis. Mol. Microbiol. 7: 967 974.
56. Trach, K.,, D. Burbulys,, M. Strauch,, J.-J. Wu,, N. Dhillon,, R. Jonas,, C. Hanstein,, R. Kallio,, M. Perego,, T. Bird,, G. Spiegelman,, C. Fogher,, and J. A. Hoch. 1991. Control of the initiation of sporulation in Bacillus subtilis by a phosphorelay. Res. Microbiol. 142: 815 823.
57. Trach, K.,, J. W. Chapman,, P. Piggot,, D. LeCoq,, and J. A. Hoch. 1988. Complete sequence and transcriptional analysis of the spo0F region of the Bacillus subtilis chromosome. J. Bacteriol. 170: 4194 4208.
58. Trach, K.,, and J. A. Hoch. 1989. The Bacillus subtilis spo0B stage 0 sporulation operon encodes an essential GTP-binding protein. J. Bacteriol. 171: 1362 1371.
59. Trach, K. A.,, and J. A. Hoch. 1993. Multisensory activation of the phosphorelay initiating sporulation in Bacillus subtilis: identification and sequence of the protein kinase of the alternate pathway. Mol. Microbiol. 8: 69 79.
60. Volz, K.,, and P. Matsumura. 1991. Crystal structure of Escherichia coli CheY refined at 1.7-A resolution. J. Biol. Chem. 266: 15511 15519.
61. Walton, K. M.,, and J. E. Dixon. 1993. Protein tyrosine phosphatases. Annu. Rev. Biochem. 62: 101 120.
62. Weinrauch, Y.,, R. Penchev,, E. Dubnau,, I. Smith,, and D. Dubnau. 1990. A Bacillus subtilis regulatory gene product for genetic competence and sporulation resembles sensor protein members of the bacterial two-component signal-transduction systems. Genes Dev. 4: 860 872.
63. Weir, J.,, M. Predich,, E. Dubnau,, G. Nair,, and I. Smith. 1991. Regulation of spo0H, a gene coding for the Bacillus subtilis σ H factor. J. Bacteriol. 173: 521 529.
64. Welsh, K. M.,, K. A. Trach,, C. Folger,, and J. A. Hoch. 1994. Biochemical characterization of the essential GTP-binding protein Obg of Bacillus subtilis J. Bacteriol. 176: 7161 7168.
65. Yamashita, S.,, F. Kawamura,, H. Yoshikawa,, H. Takahashi,, Y. Kobayashi,, and H. Saito. 1989. Dissection of the expression signals of the spo0A gene of Bacillus subtilis: glucose represses sporulation- specific expression. J. Gen. Microbiol. 135: 1335 1345.
66. York, K.,, T. J. Kenney,, S. Satola,, C. P. Moran, Jr.,, H. Poth,, and P. Youngman. 1992. Spo0A controls the σ A-dependent activation of Bacillus subtilis sporulation-specific transcription unit spoIIE. J. Bacteriol. 174: 2648 2658.
67. Zapf, J. Unpublished data.

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