RemA (YlzA) and RemB (YaaB) regulate extracellular matrix operon expression and biofilm formation in Bacillus subtilis

Journal of Bacteriology

Volumn 191, Issue 12, 2009, Pages 3981-3991

  Winkelman, Jared T ^a,b   Blair, Kris M ^a   Kearns, Daniel B ^a  

^a INDIANA UNIVERSITY   (United States)

^b UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; PROTEIN SINR; PROTEIN TASA; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR REMA; TRANSCRIPTION FACTOR REMB; UNCLASSIFIED DRUG;

ARTICLE; BACILLUS SUBTILIS; BACTERIAL MUTATION; BACTERIAL STRAIN; BIOFILM; CELL MOTILITY; CONTROLLED STUDY; EXTRACELLULAR MATRIX; GENE ACTIVATION; GENE EXPRESSION; NONHUMAN; OPERON; PRIORITY JOURNAL; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PHYSIOLOGY;

BACILLUS SUBTILIS; OCTODON DEGUS;

BACILLUS SUBTILIS; BACTERIAL PROTEINS; BIOFILMS; EXTRACELLULAR MATRIX; GENE EXPRESSION REGULATION, BACTERIAL; OPERON;

EID: 67549119039     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.00278-09     Document Type: Article

References (51)

1. Alonso, J. C., and G. Lüder. 1991. Characterization of recF suppressors in Bacillus subtilis. Biochimie 73:277-280.
2. 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.
3. Ayora, S., and J. C. Alonso. 1997. Purification and characterization of the RecF protein from Bacillus subtilis 168. Nucleic Acids Res. 25:2766-2772.
4. Bai, U., I. Mandic-Mulec, and I. Smith. 1993. SinI modulates the activity of SinR, a developmental switch protein of Bacillus subtilis, by protein-protein interaction. Genes Dev. 7:139-148.
5. Banse, A. V., A. Chastanet, L. Rahn-Lee, E. C. Hobbs, and R. Losick. 2008. Parallel pathways of repression and antirepression governing the transition to stationary phase in Bacillus subtilis. Proc. Natl. Acad. Sci. USA 105:15547-15552.
6. Blair, K. M., L. Turner, J. T. Winkelman, H. C. Berg, and D. B. Kearns. 2008. A molecular clutch disables flagella in the Bacillus subtilis biofilm. Science 320:1636-1638.
7. Branda, S. S., F. Chu, D. B. Kearns, R. Losick, and R. Kolter. 2006. A major component of the Bacillus subtilis biofilm matrix. Mol. Microbiol. 59:1229-1238.
8. Branda, S. S., J. E. González-Pastor, S. Ben-Yehuda, R. Losick, and R. Kolter. 2001. Fruiting Body Formation by Bacillus subtilis. Proc. Natl. Acad. Sci. USA 98:11621-11626.
9. Branda, S. S., J. E. González-Pastor, E. Dervyn, S. D. Ehrlich, R. Losick, and R. Kolter. 2004. Genes involved in formation of structured multicellular communities by Bacillus subtilis. J. Bacteriol. 186:3970-3979.
10. Burgess, R. R. 1969. Separation and characterization of the subunits of RNA polymerase. J. Biol. Chem. 244:2168-2176.
11. Chai, Y., F. Chu, R. Kolter, and R. Losick. 2008. Bistability and biofilm formation in Bacillus subtilis. Mol. Microbiol. 67:254-263.
12. Chu, F., D. B. Kearns, S. S. Branda, R. Kolter, and R. Losick. 2006. Targets of the master regulator of biofilm formation in Bacillus subtilis. Mol. Microbiol. 59:1216-1228.
13. Chu, F., D. B. Kearns, A. McLoon, Y. Chai, R. Kolter, and R. Losick. 2008. A novel regulatory protein governing biofilm formation in Bacillus subtilis. Mol. Microbiol. 68:1117-1127.
14. Fujita, M., J. E. González-Pastor, and R. Losick. 2005. High- and low-threshold genes in the Spo0A regulation of Bacillus subtilis. J. Bacteriol. 187:1357-1368.
15. 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.
16. Gentry, D. R., and R. R. Burgess. 1989. rpoZ, encoding the omega subunit of Escherichia coli RNA polymerase, is in the same operon as spoT. J. Bacteriol. 171:1271-1277. (Pubitemid 19080762)
17. Gentry, D., H. Xiao, R. Burgess, and M. Cashel. 1991. The omega subunit of Escherichia coli K-12 RNA polymerase is not required for stringent RNA control in vivo. J. Bacteriol. 173:3901-3903.
18. Gentry, D., C. Bengra, K. Ikehara, and M. Cashel. 1993. Guanylate kinase of Escherichia coli K-12. J. Biol. Chem. 268:14316-14321.
19. Göttler, T., and D. Klostermeier. 2007. Dissection of the nucleotide cycle of B. subtilis DNA gyrase and its modulation by DNA. J. Mol. Biol. 367:1392-1404.
20. Guérout-Fleury, A.-M., N. Frandsen, and P. Stragier. 1996. Plasmids for ectopic integration in Bacillus subtilis. Gene 180:57-61.
21. Hamon, M. A., and B. A. Lazazzera. 2001. The sporulation transcription factor Spo0A is required for biofilm development in Bacillus subtilis. Mol. Microbiol. 42:1199-1209. (Pubitemid 34209082)
22. Hamon, M. A., N. R. Stanley, R. A. Britton, A. D. Grossman, and B. A. Lazazzera. 2004. Identification of AbrB-regulated genes involved in biofilm formation by Bacillus subtilis. Mol. Microbiol. 52:847-860.
23. Haugen, S. P., W. Ross, M. Manrique, and R. L. Gourse. 2008. Fine structure of the promoter-sigma region 1.2 interaction. Proc. Natl. Acad. Sci. USA 105:3293-3297.
24. Igarashi, K., N. Fujita, and A. Ishihama. 1986. Promoter selectivity of Escherichia coli RNA polymerase: omega factor is responsible for the ppGpp sensitivity. Nucleic Acids Res. 17:8755-8765.
25. Kearns, D. B., F. Chu, S. S. Branda, R. Kolter, and R. Losick. 2005. A master regulator of biofilm formation by Bacillus subtilis. Mol. Microbiol. 55:739-749.
26. Kearns, D. B., and R. Losick. 2003. Swarming motility in undomesticated Bacillus subtilis. Mol. Microbiol. 49:581-590.
27. Kobayashi, K. 2007. Gradual activation of the response regulator DegU controls serial expression of genes for flagellum formation and biofilm formation in Bacillus subtilis. Mol. Microbiol. 66:395-409. (Pubitemid 47482381)
28. Kobayashi, K., R. Kuwana, and H. Takamatsu. 2008. kinA mRNA is missing a stop codon in the undomesticated Bacillus subtilis strain ATCC 6051. Microbiol. 154:54-63.
29. Kobayashi, K. 2008. SlrR/SlrA controls the initiation of biofilm formation in Bacillus subtilis. Mol. Microbiol. 69:1399-1410.
30. Kobayashi, K., S. D. Ehrlich, A. Albertini, G. Amati, K. K. Andersen, M. Araund, K. Asai, et al. 2003. Essential Bacillus subtilis genes. Proc. Natl. Acad. Sci. USA 100:4678-4683.
31. Kolter, R., and E. P. Greenberg. 2006. The superficial life of microbes. Nature 441:300-303.
32. Krásný, L., and R. L. Gourse. 2004. An alternative strategy for bacterial ribosome synthesis: Bacillus subtilis rRNA transcription regulation. EMBO J. 23:4473-4483.
33. Le Breton, Y., N. P. Mohapatra, and W. G. Haldenwang. 2006. In vivo random mutagenesis of Bacillus subtilis by use of TnYLB-1 a mariner-based transposon. Appl. Environ. Microbiol. 72:327-333.
34. Levano-Garcia, J., S. Verjovski-Almeida, and A. C. R. da Silva. 2005. Mapping transposon insertion sties by touchdown PCR and hybrid degenerate primers. BioTechniques 38:225-229.
35. López, D., M. A. Fischbach, F. Chu, R. Losick, and R. Kolter. 2009. Structurally diverse natural products that cause potassium leakage trigger multicellularity in Bacillus subtilis. Proc. Natl. Acad. Sci. USA 106:280-285.
36. Lopez, J. M., C. L. Marks, and E. Freese. 1979. The decrease of guanine nucleotides initiates sporulation of Bacillus subtilis. Biochim. Biophys. Acta 587:238-252.
37. Mathew, R., R. Mukherjee, R. Balachandar, and D. Chatterji. 2006. Deletion of the rpoZ gene, encoding the subunit of RNA polymerase, results in pleiotropic surface-related phenotypes in Mycobacterium smegmatis. Microbiology 152:1741-1750.
38. Orr, E., and W. L. Staudenbauer. 1982. Bacillus subtilis DNA gyrase: puri- fication of subunits and reconstitution of supercoiling activity. J. Bacteriol. 151:524-527.
39. Paul, B. J., M. M. Barker, W. Ross, D. A. Schneider, C. Webb, J. W. Foster, and R. L. Gourse. 2004. DksA: a critical component of the transcription initiation machinery that potentiates the regulation of rRNA promoters by ppGpp and initiating NTP. Cell 118:311-322. (Pubitemid 39061112)
40. Paul, B. J., M. B. Berkman, and R. L. Gourse. 2005. DksA potentiates direct activation of amino acid promoters by ppGpp. Proc. Natl. Acad. Sci. USA 102:7823-7828.
41. Ratnayake-Lecamwasam, M., P. Serror, K.-W. Wong, and A. L. Sonenshein. 2001. Bacillus subtilis CodY represses early-stationary-phase genes by sensing GTP levels. Genes Dev. 15:1093-1103.
42. Sanchez, H., B. Carrasco, M. C. Cozar, and J. C. Alonso. 2007. Bacillus subtilis RecG branch migration translocase is required for DNA repair and chromosomal segregation. Mol. Microbiol. 65:920-935.
43. Stöver, A. G., and A. Driks. 1999. Secretion, localization, and antibacterial activity of TasA, a Bacillus subtilis spore-associated protein. J. Bacteriol. 181:1664-1672.
44. Stöver, A. G., and A. Driks. 1999. Regulation of synthesis of the Bacillus subtilis transition-phase, spore associated antibacterial protein TasA. J. Bacteriol. 181:5476-5481.
45. Stöver, A. G., and A. Driks. 1999. Control of synthesis and secretion of the Bacillus subtilis protein YqxM. J. Bacteriol. 181:7065-7069.
46. Veening, J. W., O. P. Kuipers, S. Brul, K. J. Hellingwerf, and R. Kort. 2006. Effects of phosphorelay perturbations on architecture, sporulation, and spore resistance in biofilms of Bacillus subtilis. J. Bacteriol. 188:3099-3109.
47. Verhamme, D. T., T. B. Kiley, and N. R. Stanley-Wall. 2007. DegU coordinates multicellular behavior exhibited by Bacillus subtilis. Mol. Microbiol. 65:554-568.
48. Verhamme, D. T., E. J. Murray, and N. R. Stanley-Wall. 2009. DegU and Spo0A jointly control transcription of two loci required for complex colony development by Bacillus subtilis. J. Bacteriol. 191:100-108.
49. Vlamakis, H., C. Aguilar, R. Losick, and R. Kolter. 2008. Control of cell fate by the formation of an architecturally complex bacterial community. Genes Dev. 22:945-953.
50. Vrentas, C. E., T. Gaal, W. Ross, R. H. Ebright, and R. L. Gourse. 2005. Response of RNA polymerase to ppGpp: requirement for the ω subunit and relief of this requirement by DksA. Genes Dev. 19:2378-2387. (Pubitemid 41396914)
51. Yasbin, R. E., and F. E. Young. 1974. Transduction in Bacillus subtilis by bacteriophage SPP1. J. Virol. 14:1343-1348.