Expression of the chaplin and rodlin hydrophobic sheath proteins in Streptomyces venezuelae is controlled by σ BldN and a cognate anti-sigma factor, RsbN

Molecular Microbiology

Volumn 84, Issue 6, 2012, Pages 1033-1049

  Bibb, Maureen J ^a   Domonkos, Ágota ^a,b   Chandra, Govind ^a   Buttner, Mark J ^a  

^a NORWICH RESEARCH PARK   (United Kingdom)

^b SZENT ISTVÁN UNIVERSITY   (Hungary)

Author keywords

[No Author keywords available]

Indexed keywords

CHAPLIN; FUNGAL PROTEIN; RODLIN; SIGMA FACTOR; UNCLASSIFIED DRUG;

ARTICLE; BLDN GENE; CHAPLIN GENE; CONTROLLED STUDY; FUNGAL GENE; FUNGUS CULTURE; GENE DISRUPTION; GENE EXPRESSION REGULATION; GENE FUNCTION; GENE INDUCTION; GENE INTERACTION; GENE TARGETING; HYDROPHOBICITY; MICROARRAY ANALYSIS; NONHUMAN; PRIORITY JOURNAL; RODLIN GENE; RSBN GENE; SPOROGENESIS; STREPTOMYCES VENEZUELAE;

BACTERIAL PROTEINS; BASE SEQUENCE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, BACTERIAL; GENE ORDER; MICROARRAY ANALYSIS; MODELS, BIOLOGICAL; MOLECULAR SEQUENCE DATA; SIGMA FACTOR; STREPTOMYCES;

STREPTOMYCES; STREPTOMYCES VENEZUELAE;

EID: 84865161579     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2012.08070.x     Document Type: Article

References (72)

1. Bailey, T.L., and Elkan, C. (1994) Fitting a mixture model by expectation maximization to discover motifs in biopolymers. In Proceedings of the Second International Conference on Intelligent Systems for Molecular Biology. Menlo Park: AAAI Press, pp. 28-36.
2. BldN, an extracytoplasmic function RNA polymerase sigma factor required for aerial mycelium formation in Streptomyces coelicolor A3(2). J Bacteriol 182: 4606-4616.
3. Buttner, M.J., Fearnley, I.M., and Bibb, M.J. (1987) The agarase gene (dagA) of Streptomyces coelicolor A3(2): nucleotide sequence and transcriptional analysis. Mol Gen Genet 209: 101-109.
4. Campbell, E.A., Greenwell, R., Anthony, J.R., Wang, S., Lim, L., Das, K., et al. (2007) A conserved structural module regulates transcriptional responses to diverse stress signals in bacteria. Mol Cell 27: 793-805.
5. Campbell, E.A.,Westblade, L.F., and Darst, S.A. (2008) Regulation of bacterial RNA polymerase sigma factor activity: a structural perspective. Curr Opin Microbiol 11: 121-127.
6. Capstick, D.S., Willey, J.M., Buttner, M.J., and Elliot, M.A. (2007) SapB and the chaplins: connections between morphogenetic proteins in Streptomyces coelicolor. Mol Microbiol 64: 602-613.
7. Capstick, D.S., Jomaa, A., Hanke, C., Ortega, J., and Elliot, M.A. (2011) Dual amyloid domains promote differential functioning of the chaplin proteins during Streptomyces aerial morphogenesis. Proc Natl Acad Sci USA 108: 9821-9826.
8. Chandra, G., and Chater, K.F. (2008) Evolutionary flux of potentially bldA-dependent Streptomyces genes containing the rare leucine codon TTA. Antonie Van Leeuwenhoek 94: 111-126.
9. Chater, K.F., and Chandra, G. (2008) The use of the rare UUA codon to define 'expression space' for genes involved in secondary metabolism, development and environmental adaptation in Streptomyces. J Microbiol 46: 1-11.
10. Chater, K.F., and Horinouchi, S. (2003) Signalling early developmental events in two highly diverged Streptomyces species. Mol Microbiol 48: 9-15.
11. Claessen, D., Wösten, H.A.B., van Keulen, G., Faber, O.G., Alves, A.M.C.R., Meijer, W.G., and Dijkhuizen, L. (2002) Two novel homologous proteins of Streptomyces coelicolor and Streptomyces lividans are involved in the formation of the rodlet layer and mediate attachment to a hydrophobic surface. Mol Microbiol 44: 1483-1492.
12. Claessen, D., Rink, R., de Jong, W., Siebring, J., de Vreugd, P., Boersma, F.G., et al. (2003) A novel class of secreted hydrophobic proteins is involved in aerial hyphae formation in Streptomyces coelicolor by forming amyloid-like fibrils. Genes Dev 17: 1714-1726.
13. Claessen, D., Stokroos, I., Deelstra, H.J., Penninga, N.A., Bormann, C., Salas, J.A., et al. (2004) The formation of the rodlet layer of streptomycetes is the result of the interplay between rodlins and chaplins. Mol Microbiol 53: 433-443.
14. Claessen, D., de Jong, W., Dijkhuizen, L., and Wösten, H.A. (2006) Regulation of Streptomyces development: reach for the sky! Trends Microbiol 14: 313-319.
15. Datsenko, K.A., and Wanner, B.L. (2000) One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc Natl Acad Sci USA 97: 6640-6645.
16. Di Berardo, C., Capstick, D.S., Bibb, M.J., Findlay, K.C., Buttner, M.J., and Elliot, M.A. (2008) Function and redundancy of the chaplin cell surface proteins in aerial hypha formation, rodlet assembly, and viability in Streptomyces coelicolor. J Bacteriol 190: 5879-5889.
17. Duong, A., Capstick, D.S., Di Berardo, C., Findlay, K.C., Hesketh, A., Hong, H.-J., and Elliot, M.A. (2012) Aerial development in Streptomyces coelicolor requires sortase activity. Mol Microbiol 83: 992-1005.
18. Elliot, M.A., and Talbot, N.J. (2004) Building filaments in the air: aerial morphogenesis in bacteria and fungi. Curr Opin Microbiol 7: 594-601.
19. Elliot, M.A., Bibb, M.J., Buttner, M.J., and Leskiw, B.K. (2001) BldD is a direct regulator of key developmental genes in Streptomyces coelicolor A3(2). Mol Microbiol 40: 257-269.
20. Elliot, M.A., Karoonuthaisiri, N., Huang, J., Bibb, M.J., Cohen, S.N., Kao, C.M., and Buttner, M.J. (2003) The chaplins: a family of hydrophobic cell-surface proteins involved in aerial mycelium formation in Streptomyces coelicolor. Genes Dev 17: 1727-1740.
21. Elliot, M.A., Buttner, M.J., and Nodwell, J.R. (2008) Multicellular development in Streptomyces. In Myxobacteria: Multicellularity and Differentiation. Whitworth, D.E. (ed.). Washington, DC: ASM Press, pp. 419-438.
22. Flärdh, K., and Buttner, M.J. (2009) Streptomyces morphogenetics: dissecting differentiation in a filamentous bacterium. Nat Rev Microbiol 7: 36-49.
23. Foulston, L., and Bibb, M. (2011) Feed-forward regulation of microbisporicin biosynthesis in Microbispora corallina. J Bacteriol 193: 3064-3071.
24. Glazebrook, M., Doull, J., Stuttard, C., and Vining, L. (1990) Sporulation of Streptomyces venezuelae in submerged cultures. Microbiology 136: 581-588.
25. Gregory, M.A., Till, R., and Smith, M.C.M. (2003) Integration site for Streptomyces phage FBT1 and development of site-specific integrating vectors. J Bacteriol 185: 5320-5323.
26. Gust, B., Challis, G.L., Fowler, K., Kieser, T., and Chater, K.F. (2003) PCR-targeted Streptomyces gene replacement identifies a protein domain needed for biosynthesis of the sesquiterpene soil odor geosmin. Proc Natl Acad Sci USA 100: 1541-1546.
27. Gust, B., Chandra, G., Jakimowicz, D., Yuqing, T., Bruton, C., and Chater, K.F. (2004) Lambda red-mediated genetic manipulation of antibiotic-producing Streptomyces. Adv Appl Microbiol 54: 107-128.
28. Helmann, J.D. (1999) Anti-sigma factors. Curr Opin Microbiol 2: 135-141.
29. Helmann, J.D. (2002) The Extracytoplasmic Function (ECF) sigma factors. Adv Microb Physiol 46: 47-110.
30. Helmann, J.D. (2011) Regulation by alternative sigma factors. In Bacterial Stress Responses, 2nd edn. Storz, G., and Hengge, R. (eds). Washington, DC: ASM press, pp. 31-41.
31. den Hengst, C.D., and Buttner, M.J. (2008) Redox control in actinobacteria. Biochim Biophys Acta 1780: 1201-1216.
32. den Hengst, C.D., Tran, N.T., Bibb, M.J., Chandra, C., Leskiw, B.K., and Buttner, M.J. (2010) Genes essential for morphological development and antibiotic production in Streptomyces coelicolor are targets of BldD during vegetative growth. Mol Microbiol 78: 361-379.
33. Hesketh, A., Kock, H., Mootien, S., and Bibb, M. (2009) The role of absC, a novel regulatory gene for secondary metabolism, in zinc-dependent antibiotic production in Streptomyces coelicolor A3(2). Mol Microbiol 74: 1427-1444.
34. Higo, A., Horinouchi, S., and Ohnishi, Y. (2011) Strict regulation of morphological differentiation and secondary metabolism by a positive feedback loop between two global regulators AdpA and BldA in Streptomyces griseus. Mol Microbiol 81: 1607-1622.
35. Higo, A., Hara, H., Horinouchi, S., and Ohnishi, Y. (2012) Genome-wide distribution of AdpA, a global regulator for secondary metabolism and morphological differentiation in Streptomyces, revealed the extent and complexity of the AdpA regulatory network. DNA Res. doi:10.1093/dnares/dss010
36. Hirano, S., Kato, J.Y., Ohnishi, Y., and Horinouchi, S. (2006) Control of the Streptomyces subtilisin inhibitor gene by AdpA in the A-factor regulatory cascade in Streptomyces griseus. J Bacteriol 188: 6207-6216.
37. Hopwood, D.A., and Glauert, A.M. (1961) Electron microscope observations on the surface structures of Streptomyces violaceoruber. J Gen Microbiol 26: 325-330.
38. Horinouchi, S. (2007) Mining and polishing of the treasure trove in the bacterial genus Streptomyces. Biosci Biotechnol Biochem 71: 283-299.
39. Horinouchi, S. (2008) The A-factor regulatory cascade that triggers secondary metabolism and morphological differentiation in Streptomyces. In Chemical Communication among Bacteria. Winans, S.C., and Bassler, B.L. (eds). Herndon, VA: ASM Press, pp. 363-377.
40. de Jong, W., Wösten, H.A.B., Dijkhuizen, L., and Claessen, D. (2009) Attachment of Streptomyces coelicolor is mediated by amyloidal fimbriae that are anchored to the cell surface via cellulose. Mol Microbiol 73: 1128-1140.
41. Karimova, G., Pidoux, J., Ullmann, A., and Ladant, D. (1998) A bacterial two-hybrid system based on a reconstitutedsignal transduction pathway. Proc Natl Acad Sci USA 95: 5752-5756.
42. Karimova, G., Ullmann, A., and Ladant, D. (2001) Proteinprotein interaction between Bacillus stearothermophilus tyrosyl-tRNA synthetase subdomains revealed by a bacterial two-hybrid system. J Mol Microbiol Biotechnol 3: 73-82.
43. Kieser, T., Bibb, M.J., Buttner, M.J., Chater, K.F., and Hopwood, D.A. (2000) Practical Streptomyces Genetics. Norwich: The John Innes Foundation.
44. Kim, M.S., Hahn, M.Y., Cho, Y., Cho, S.N., and Roe, J.H. (2009) Positive and negative feedback regulatory loops of thiol-oxidative stress response mediated by an unstable isoform of sR in actinomycetes. Mol Microbiol 73: 815-825.
45. Kodani, S., Hudson, M.E., Durrant, M.C., Buttner, M.J., Nodwell, J.R., and Willey, J.M. (2004) The SapB morphogen is a lantibiotic-like peptide derived from the product of the developmental gene ramS in Streptomyces coelicolor. Proc Natl Acad Sci USA 101: 11448-11453.
46. Ma, H., and Kendall, K. (1994) Cloning and analysis of a gene cluster from Streptomyces coelicolor that causes accelerated aerial mycelium formation in Streptomyces lividans. J Bacteriol 176: 3800-3811.
47. McCormick, J.R., and Flärdh, K. (2012) Signals and regulators that govern Streptomyces development. FEMS Microbiol Rev 36: 206-231.
48. Molle, V., and Buttner, M.J. (2000) Different alleles of the response regulator gene bldM arrest Streptomyces coelicolor development at distinct stages. Mol Microbiol 36: 1265-1278.
49. Nash, H.A., Robertson, C.A., Flamm, E., Weisberg, R.A., and, Miller, H.I. (1987) Overproduction of Escherichia coli integration host factor, a protein with nonidentical subunits. J Bacteriol 169: 4124-4127.
50. Ohnishi, Y., Yamazaki, H., Kato, J.-Y., Tomono, A., and Horinouchi, S. (2005) AdpA, a central transcriptional regulator in the A-factor regulatory cascade that leads to morphological development and secondary metabolism in Streptomyces griseus. Biosci Biotechnol Biochem 69: 431-439.
51. Paget, M.S., and Buttner, M.J. (2003) Thiol-based regulatory switches. Annu Rev Genet 37: 91-121.
52. Paget, M.S.B., Kang, J.-G., Roe, J.-H., and Buttner, M.J. (1998) sR, an RNA polymerase sigma factor that modulates expression of the thioredoxin system in response to oxidative stress in Streptomyces coelicolor A3(2). EMBO J 17: 5776-5782.
53. Paget, M.S.B., Chamberlin, L., Atrih, A., Foster, S.J., and Buttner, M.J. (1999) Evidence that the extracytoplasmic function sigma factor, sE, is required for normal cell wall structure in Streptomyces coelicolor A3(2). J Bacteriol 181: 204-211.
54. Park, J.H., and Roe, J.H. (2008) Mycothiol regulates and is regulated by a thiol-specific antisigma factor RsrA and sR in Streptomyces coelicolor. Mol Microbiol 68: 861-870.
55. Pullan, S.T., Chandra, G., Bibb, M.J., and Merrick, M. (2011) Genome-wide analysis of the role of GlnR in Streptomyces venezuelae provides new insights into global nitrogen regulation in actinomycetes. BMC Genomics 12: 175.
56. Raman, S., Hazra, R., Dascher, C.C., and Husson, R.N. (2004) Transcription regulation by the Mycobacterium tuberculosis alternative sigma factor SigD and its role in virulence. J Bacteriol 186: 6605-6616.
57. Sawyer, E.B., Claessen, D., Haas, M., Hurgobin, B., and Gras, S.L. (2011) The assembly of individual chaplin peptides from Streptomyces coelicolor into functional amyloid fibrils. PLoS ONE 6: e18839.
58. Slavny, P., Little, R., Salinas, P., Clarke, T.A., and Dixon, R. (2010) Quaternary structure changes in a second Per-Arnt-Sim domain mediate intramolecular redox signal relay in the NifL regulatory protein. Mol Microbiol 75: 61-75.
59. Staron , A., Sofia, H.J., Dietrich, S., Ulrich, L.E., Liesegang, H., and Mascher, T. (2009) The third pillar of bacterial signal transduction: classification of the extracytoplasmic function (ECF) sigma factor protein family. Mol Microbiol 74: 557-581.
60. Stuttard, C. (1979) Transduction of auxotrophic markers in a chloramphenicol-producing strain of Streptomyces. J Gen Microbiol 110: 479-482.
61. Stuttard, C. (1982) Temperate phages of Streptomyces venezuelae: lysogeny and host specificity shown by phages SV1 and SV2. Microbiology 128: 115-121.
62. Takano, E., Tao, M., Long, F., Bibb, M.J., Wang, L., Li, W., et al. (2003) A rare leucine codon in adpA is implicated in the morphological defect of bldA mutants of Streptomyces coelicolor. Mol Microbiol 50: 475-486.
63. Tillotson, R.D., Wosten, H.A., Richter, M., and Willey, J.M. (1998) A surface active protein involved in aerial hyphae formation in the filamentous fungus Schizophillum commune restores the capacity of a bald mutant of the filamentous bacterium Streptomyces coelicolor to erect aerial structures. Mol Microbiol 30: 595-602.
64. Tomono, A., Tsai, Y., Yamazaki, H., Ohnishi, Y., and Horinouchi, S. (2005a) Transcriptional control by A-factor of strR, the pathway-specific transcriptional activator for streptomycin biosynthesis in Streptomyces griseus. J Bacteriol 187: 5595-5604.
65. Tomono, A., Tsai, Y., Ohnishi, Y., and Horinouchi, S. (2005b) Three chymotrypsin genes are members of the AdpA regulon in the A-factor regulatory cascade in Streptomyces griseus. J Bacteriol 187: 6341-6353.
66. Wildermuth, H., Wehrli, E., and Horne, R.W. (1971) The surface structure of spores and aerial mycelium in Streptomyces coelicolor. J Ultrastruct Res 35: 168-180.
67. Willey, J., Santamaria, R., Guijarro, J., Geistlich, M., and Losick, R. (1991) Extracellular complementation of a developmental mutation implicates a small sporulation protein in aerial mycelium formation by S. coelicolor. Cell 65: 641-650.
68. Willey, J.M., Willems, A., Kodani, S., and Nodwell, J.R. (2006) Morphogenetic surfactants and their role in the formation of aerial hyphae in Streptomyces coelicolor. Mol Microbiol 59: 731-742.
69. Yamazaki, H., Ohnishi, Y., and Horinouchi, S. (2000) An A-factor-dependent extracytoplasmic function sigma factor (sAdsA) that is essential for morphological development in Streptomyces griseus. J Bacteriol 182: 4596-4605.
70. Yamazaki, H., Ohnishi, Y., and Horinouchi, S. (2003a) Transcriptional switch on of ssgA by A-factor, which is essential for spore septum formation in Streptomyces griseus. J Bacteriol 185: 1273-1283.
71. Yamazaki, H., Takano, Y., Ohnishi, Y., and Horinouchi, S. (2003b) amfR, an essential gene for aerial mycelium formation, is a member of the AdpA regulon in the A-factor regulatory cascade in Streptomyces griseus. Mol Microbiol 50: 1173-1187.
72. Yamazaki, H., Tomono, A., Ohnishi, Y., and Horinouchi, S. (2004) DNA-binding specificity of AdpA, a transcriptional activator in the A-factor regulatory cascade in Streptomyces griseus. Mol Microbiol 53: 555-572.