Novel modulators controlling entry into sporulation in Bacillus subtilis

Journal of Bacteriology

Volumn 195, Issue 7, 2013, Pages 1475-1483

  Garti levi, Sharon ^a   Eswara, Ashlee ^b,c   Smith, Yoav ^a   Fujita, Masaya ^b   Ben Yehuda, Sigal ^a  

^a HEBREW UNIVERSITY   (Israel)

^b University of Houston   (United States)

^c CENTER FOR BIOLOGICS EVALUATION AND RESEARCH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; BACILLUS SUBTILIS; GENE; GENE CONTROL; GENE IDENTIFICATION; GENETIC CODE; GENETIC TRANSCRIPTION; GROWTH; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; SPOROGENESIS; UPREGULATION;

BACILLUS SUBTILIS; BACTERIAL PROTEINS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, BACTERIAL; PROTEIN KINASES; SIGNAL TRANSDUCTION; SPORES, BACTERIAL; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC;

BACILLUS SUBTILIS;

EID: 84875496227     PISSN: 00219193     EISSN: 10985530     Source Type: Journal    
DOI: 10.1128/JB.02160-12     Document Type: Article

References (50)

1. Piggot PJ, Hilbert DW. 2004. Sporulation of Bacillus subtilis. Curr. Opin. Microbiol. 7:579 -586.
2. Higgins D, Dworkin J. 2012. Recent progress in Bacillus subtilis sporulation. FEMS Microbiol. Rev. 36:131-148.
3. Errington J. 1996. Determination of cell fate in Bacillus subtilis. Trends Genet. 12:31-34.
4. Stragier P, Losick R. 1996. Molecular genetics of sporulation in Bacillus subtilis. Annu. Rev. Genet. 30:297-341.
5. Sonenshein AL. 2000. Control of sporulation initiation in Bacillus subtilis. Curr. Opin. Microbiol. 3:561-566.
6. Burbulys D, Trach KA, Hoch JA. 1991. Initiation of sporulation in B. subtilis is controlled by a multicomponent phosphorelay. Cell 64:545-552.
7. Hoch JA. 1993. The phosphorelay signal transduction pathway in the initiation of Bacillus subtilis sporulation. J. Cell. Biochem. 51:55- 61.
8. Perego M, Hanstein C, Welsh KM, Djavakhishvili T, Glaser P, Hoch JA. 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.
9. Burkholder WF, Kurtser I, Grossman AD. 2001. Replication initiation proteins regulate a developmental checkpoint in Bacillus subtilis. Cell 104: 269-279.
10. Wang L, Grau R, Perego M, Hoch JA. 1997. A novel histidine kinase inhibitor regulating development in Bacillus subtilis. Genes Dev. 11:2569- 2579.
11. Rowland SL, Burkholder WF, Cunningham KA, Maciejewski MW, Grossman AD, King GF. 2004. Structure and mechanism of action of Sda, an inhibitor of the histidine kinases that regulate initiation of sporulation in Bacillus subtilis. Mol. Cell 13:689 -701.
12. Jacques DA, Langley DB, Jeffries CM, Cunningham KA, Burkholder WF, Guss JM, Trewhella J. 2008. Histidine kinase regulation by a cyclophilin- like inhibitor. J. Mol. Biol. 384:422- 435.
13. Molle V, Fujita M, Jensen ST, Eichenberger P, Gonzalez-Pastor JE, Liu JS, Losick R. 2003. The Spo0A regulon of Bacillus subtilis. Mol. Microbiol. 50:1683-1701.
14. Fawcett P, Eichenberger P, Losick R, Youngman P. 2000. The transcriptional profile of early to middle sporulation in Bacillus subtilis. Proc. Natl. Acad. Sci. U. S. A. 97:8063- 8068.
15. Liu JJ, Tan K, Stormo GD. 2003. Computational identification of the Spo0A-phosphate regulon that is essential for the cellular differentiation and development in Gram-positive spore-forming bacteria. Nucleic Acids Res. 31:6891- 6903.
16. Fujita M, Gonzalez-Pastor JE, Losick R. 2005. High- and lowthreshold genes in the Spo0A regulon of Bacillus subtilis. J. Bacteriol. 187:1357-1368.
17. Fujita M, Losick R. 2005. Evidence that entry into sporulation in Bacillus subtilis is governed by a gradual increase in the level and activity of the master regulator Spo0A. Genes Dev. 19:2236 -2244.
18. Chibazakura T, Kawamura F, Asai K, Takahashi H. 1995. Effects of spo0 mutations on spo0A promoter switching at the initiation of sporulation in Bacillus subtilis. J. Bacteriol. 177:4520-4523.
19. Chibazakura T, Kawamura F, Takahashi H. 1991. Differential regulation of spo0A transcription in Bacillus subtilis: glucose represses promoter switching at the initiation of sporulation. J. Bacteriol. 173:2625- 2632.
20. Baldus JM, Buckner CM, Moran CP, Jr. 1995. Evidence that the transcriptional activator Spo0A interacts with two sigma factors in Bacillus subtilis. Mol. Microbiol. 17:281-290.
21. Strauch MA, Trach KA, Day J, Hoch JA. 1992. Spo0A activates and represses its own synthesis by binding at its dual promoters. Biochimie 74:619-626.
22. Harwood CR, Cutting SM. 1990. Molecular biological methods for Bacillus. Wiley, New York, NY.
23. Dubey GP, Ben-Yehuda S. 2011. Intercellular nanotubes mediate bacterial communication. Cell 144: 590-600
24. Bejerano-Sagie M, Oppenheimer-Shaanan Y, Berlatzky I, Rouvinski A, Meyerovich M, Ben-Yehuda S. 2006. A checkpoint protein that scans the chromosome for damage at the start of sporulation in Bacillus subtilis. Cell 125:679-690.
25. Tjalsma H, Antelmann H, Jongbloed JD, Braun PG, Darmon E, Dorenbos R, Dubois JY, Westers H, Zanen G, Quax WJ, Kuipers OP, Bron S, Hecker M, van Dijl JM. 2004. Proteomics of protein secretion by Bacillus subtilis: separating the "secrets" of the secretome. Microbiol. Mol. Biol. Rev. 68:207-233.
26. Fujita M, 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. 124:98 -104.
27. Fujita M, 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.
28. Strauch M, Webb V, Spiegelman G, Hoch JA. 1990. The SpoOA protein of Bacillus subtilis is a repressor of the abrB gene. Proc. Natl. Acad. Sci. U. S. A. 87:1801-1805.
29. Jiang M, Shao W, Perego M, Hoch JA. 2000. Multiple histidine kinases regulate entry into stationary phase and sporulation in Bacillus subtilis. Mol. Microbiol. 38:535-542.
30. Brunsing RL, La Clair C, Tang S, Chiang C, Hancock LE, Perego M, Hoch JA. 2005. Characterization of sporulation histidine kinases of Bacillus anthracis. J. Bacteriol. 187:6972- 6981.
31. Kobayashi K, Iwano M. 2012. BslA (YuaB) forms a hydrophobic layer on the surface of Bacillus subtilis biofilms. Mol. Microbiol. 85:51- 66.
32. Kovacs AT, Kuipers OP. 2011. Rok regulates yuaB expression during architecturally complex colony development of Bacillus subtilis 168. J. Bacteriol. 193:998 -1002.
33. Ostrowski A, Mehert A, Prescott A, Kiley TB, Stanley-Wall NR. 2011. YuaB functions synergistically with the exopolysaccharide and TasA amyloid fibers to allow biofilm formation by Bacillus subtilis. J. Bacteriol. 193:4821- 4831.
34. Fabret C, Hoch JA. 1998. A two-component signal transduction system essential for growth of Bacillus subtilis: implications for anti-infective therapy. J. Bacteriol. 180:6375- 6383.
35. Fukuchi K, Kasahara Y, Asai K, Kobayashi K, Moriya S, Ogasawara N. 2000. The essential two-component regulatory system encoded by yycF and yycG modulates expression of the ftsAZ operon in Bacillus subtilis. Microbiology 146(Part 7):1573-1583.
36. Strauch MA, Wu JJ, Jonas RH, Hoch JA. 1993. A positive feedback loop controls transcription of the spoOF gene, a component of the sporulation phosphorelay in Bacillus subtilis. Mol. Microbiol. 7:967-974.
37. Predich M, Nair G, 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.
38. Antelmann H, Tjalsma H, Voigt B, Ohlmeier S, Bron S, van Dijl JM, Hecker M. 2001. A proteomic view on genome-based signal peptide predictions. Genome Res. 11:1484 -1502.
39. Perego M, Cole SP, Burbulys D, Trach K, Hoch JA. 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.
40. Eswaramoorthy P, Dinh J, Duan D, Igoshin OA, Fujita M. 2010. Single-cell measurement of the levels and distributions of the phosphorelay components in a population of sporulating Bacillus subtilis cells. Microbiology 156:2294 -2304.
41. Eswaramoorthy P, Dravis A, Devi SN, Vishnoi M, Dao HA, Fujita M. 2011. Expression level of a chimeric kinase governs entry into sporulation in Bacillus subtilis. J. Bacteriol. 193:6113- 6122.
42. Trach KA, Hoch JA. 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.
43. Dartois V, Djavakhishvili T, Hoch JA. 1997. KapB is a lipoprotein required for KinB signal transduction and activation of the phosphorelay to sporulation in Bacillus subtilis. Mol. Microbiol. 26:1097-1108.
44. Kobayashi K, Shoji K, Shimizu T, Nakano K, Sato T, Kobayashi Y. 1995. Analysis of a suppressor mutation ssb (kinC) of sur0B20 (spo0A) mutation in Bacillus subtilis reveals that kinC encodes a histidine protein kinase. J. Bacteriol. 177:176 -182.
45. Chastanet A, Losick R. 2011. Just-in-time control of Spo0A synthesis in Bacillus subtilis by multiple regulatory mechanisms. J. Bacteriol. 193: 6366-6374.
46. Chastanet A, Vitkup D, Yuan GC, Norman TM, Liu JS, Losick RM. 2010. Broadly heterogeneous activation of the master regulator for sporulation in Bacillus subtilis. Proc. Natl. Acad. Sci. U. S. A. 107:8486 - 8491.
47. Mirouze N, Prepiak P, Dubnau D. 2011. Fluctuations in spo0A transcription control rare developmental transitions in Bacillus subtilis. PLoS Genet. 7:e1002048. doi:10.1371/journal.pgen.1002048.
48. Verhamme DT, Murray EJ, Stanley-Wall NR. 2009. DegU and Spo0A jointly control transcription of two loci required for complex colony development by Bacillus subtilis. J. Bacteriol. 191:100 -108.
49. Aguilar C, Vlamakis H, Guzman A, Losick R, Kolter R. 2010. KinD is a checkpoint protein linking spore formation to extracellular-matrix production in Bacillus subtilis biofilms. mBio 1(1):e00035-10. doi:10.1128 /mBio.00035-10.
50. Serizawa M, Yamamoto H, Yamaguchi H, Fujita Y, Kobayashi K, Ogasawara N, Sekiguchi J. 2004. Systematic analysis of SigD-regulated genes in Bacillus subtilis by DNA microarray and Northern blotting analyses. Gene 329:125-136.