Importance and regulation of inositol biosynthesis during growth and differentiation of Streptomyces

Molecular Microbiology

Volumn 83, Issue 6, 2012, Pages 1178-1194

  Zhang, Guohua ^a,c   Tian, Yuqing ^a   Hu, Kun ^a   Zhu, Yu ^a   Chater, Keith F ^b   Feng, Chi ^a   Liu, Gang ^a   Tan, Huarong ^a  

^a INSTITUTE OF MICROBIOLOGY   (China)

^b JOHN INNES CENTRE   (United Kingdom)

^c CHENGDU INSTITUTE OF BIOLOGY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

GLUCOSE 6 PHOSPHATE; INOSITOL;

ARTICLE; BACTERIAL GENE; BACTERIAL GROWTH; BACTERIAL METABOLISM; BINDING AFFINITY; BINDING SITE; CONTROLLED STUDY; GENE DELETION; INOA GENE; INOR GENE; METABOLIC REGULATION; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; REGULATOR GENE; SEQUENCE ANALYSIS; SPOROGENESIS; STREPTOMYCES COELICOLOR; TRANSCRIPTION INITIATION SITE; TRANSCRIPTION REGULATION;

BACTERIAL PROTEINS; BASE SEQUENCE; GENE EXPRESSION REGULATION, BACTERIAL; INOSITOL; MOLECULAR SEQUENCE DATA; MYO-INOSITOL-1-PHOSPHATE SYNTHASE; PROMOTER REGIONS, GENETIC; PROTEIN BINDING; SPORES, BACTERIAL; STREPTOMYCES COELICOLOR;

ACTINOBACTERIA; STREPTOMYCES; STREPTOMYCES COELICOLOR;

EID: 84862810528     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2012.08000.x     Document Type: Article

References (47)

1. Ainsa, J.A., Parry, H.D., and Chater, K.F. (1999) A response regulator-like protein that functions at an intermediate stage of sporulation in Streptomyces coelicolor A3(2). Mol Microbiol 34: 607-619.
2. Bennett, B.D., Kimball, E.H., Gao, M., Osterhout, R., VanDien, S.J., and Rabinowitz, J.D. (2009) Absolute metabolite concentrations and implied enzyme active site occupancy in Escherichia coli. Nat Chem Biol 5: 593-599.
3. Bentley, S.D., Chater, K.F., Cerdeno-Tarraga, A.M., Challis, G.L., Thomson, N.R., James, K.D., etal. (2002) Complete genome sequence of the model actinomycete Streptomyces coelicolor A3(2). Nature 417: 141-147.
4. Besra, G.S., Morehouse, C.B., Rittner, C.M., Waechter, C.J., and Brennan, P.J. (1997) Biosynthesis of mycobacterial lipoarabinomannan. J Biol Chem 272: 18460-18466.
5. Bucala, R., Model, P., and Cerami, A. (1984) Modification of DNA by reducing sugars: a possible mechanism for nucleic acid aging and age-related dysfunction in gene expression. Proc Natl Acad Sci USA 81: 105-109.
6. Chater, K.F. (1993) Genetics of differentiation in Streptomyces. Annu Rev Microbiol 47: 685-713.
7. Chater, K.F. (2001) Regulation of sporulation in Streptomyces coelicolor A3(2): a checkpoint multiplex? Curr Opin Microbiol 4: 667-673.
8. Chouayekh, H., Nothaft, H., Delaunay, S., Linder, M., Payrastre, B., Seghezzi, N., etal. (2007) Phosphoinositides are involved in control of the glucose-dependent growth resumption that follows the transition phase in Streptomyces lividans. J Bacteriol 189: 741-749.
9. 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.
10. Dinadayala, P., Kaur, D., Berg, S., Amin, A.G., Vissa, V.D., Chatterjee, D., etal. (2006) Genetic basis for the synthesis of the immunomodulatory mannose caps of lipoarabinomannan in Mycobacterium tuberculosis. J Biol Chem 281: 20027-20035.
11. Fahey, R.C. (2001) Novel thiols of prokaryotes. Annu Rev Microbiol 55: 333-356.
12. Flärdh, K., and Buttner, M.J. (2009) Streptomyces morphogenetics: dissecting differentiation in a filamentous bacterium. Nat Rev Microbiol 7: 36-49.
13. Flärdh, K., Leibowitz, E., Buttner, M.J., and Chater, K.F. (2000) Generation of a non-sporulating strain of Streptomyces coelicolor A3(2) by the manipulation of a developmentally controlled ftsZ promoter. Mol Microbiol 38: 737-749.
14. 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 odor geosmin. Proc Natl Acad Sci USA 100: 1541-1546.
15. Hirsch, J.P., and Henry, S.A. (1986) Expression of the Saccharomyces cerevisiae inositol-1-phosphate synthase (INO1) gene is regulated by factors that affect phospholipid synthesis. Mol Cell Biol 6: 3320-3328.
16. Hoischen, C., Gura, K., Luge, C., and Gumpert, J. (1997) Lipid and fatty acid composition of cytoplasmic membranes from Streptomyces hygroscopicus and its stable protoplast-type L form. J Bacteriol 179: 3430-3436.
17. Horton, R.M., Hunt, H.D., Ho, S.N., Pullen, J.K., and Pease, L.R. (1989) Engineering hybrid genes without the use of restriction enzymes: gene splicing by overlap extension. Gene 77: 61-68.
18. Hunter, S.W., and Brennan, P.J. (1990) Evidence for the presence of a phosphatidylinositol anchor on the lipoarabinomannan and lipomannan of Mycobacterium tuberculosis. J Biol Chem 265: 9272-9279.
19. Jackson, M., Crick, D.C., and Brennan, P.J. (2000) Phosphatidylinositol is an essential phospholipid of mycobacteria. J Biol Chem 275: 30092-30099.
20. Jyothikumar, V., Tilley, E.J., Wali, R., and Herron, P.R. (2008) Time-lapse microscopy of Streptomyces coelicolor growth and sporulation. Appl Environ Microbiol 74: 6774-6781.
21. Kalscheuer, R., Syson, K., Veeraraghavan, U., Weinrick, B., Biermann, K.E., Liu, Z., etal. (2010) Self-poisoning of Mycobacterium tuberculosis by targeting GlgE in an alpha-glucan pathway. Nat Chem Biol 6: 376-384.
22. Kieser, T., Bibb, M.J., Buttner, M.J., Chater, K.F., and Hopwood, D.A. (2000) Practical Streptomyces Genetics. A Laboratory Manual. Norwich: John Innes Foundation.
23. Korduláková, J., Gilleron, M., Mikusova, K., Puzo, G., Brennan, P.J., Gicquel, B., etal. (2002) Definition of the first mannosylation step in phosphatidylinositol mannoside synthesis. PimA is essential for growth of mycobacteria. J Biol Chem 277: 31335-31344.
24. Korduláková, J., Gilleron, M., Puzo, G., Brennan, P.J., Gicquel, B., Mikusova, K., etal. (2003) Identification of the required acyltransferase step in the biosynthesis of the phosphatidylinositol mannosides of mycobacterium species. J Biol Chem 278: 36285-36295.
25. Kukimoto, J., and Kanda, T. (2001) Displacement of YY1 by differentiation-specific transcription factor hSkn-1a activates the P(670) promoter of human papillomavirus type 16. J Virol 19: 9302-9311.
26. Kwak, J., Dharmatilake, A.J., Jiang, H., and Kendrick, K.E. (2001) Differential regulation of ftsZ transcription during septation of Streptomyces griseus. J Bacteriol 183: 5092-5101.
27. MacNeil, D.J., Gewain, K.M., Ruby, C.L., Dezeny, G., Gibbons, P.H., and MacNeil, T. (1992) Analysis of Streptomyces avermitilis genes required for avermectin biosynthesis utilizing a novel integration vector. Gene 111: 61-69.
28. Michell, R.H. (2008) Inositol derivatives: evolution and functions. Nat Rev Mol Cell Biol 9: 151-161.
29. Monnier, V.M., and Cerami, A. (1981) Nonenzymatic browning in vivo: possible process for aging of long-lived proteins. Science 211: 491-493.
30. Movahedzadeh, F., Smith, D.A., Norman, R.A., Dinadayala, P., Murray-Rust, J., Russell, D.G., etal. (2004) The Mycobacterium tuberculosis ino1 gene is essential for growth and virulence. Mol Microbiol 51: 1003-10014.
31. Newton, G.L., Arnold, K., Price, M.S., Sherrill, C., Delcardayre, S.B., Aharonowitz, Y., etal. (1996) Distribution of thiols in microorganisms: mycothiol is a major thiol in most actinomycetes. J Bacteriol 178: 1990-1995.
32. Nigou, J., Gilleron, M., Cahuzac, B., Bounery, J.D., Herold, M., Thurnher, M., etal. (1997) The phosphatidyl-myo-inositol anchor of the lipoarabinomannans from Mycobacterium bovis bacillus Calmette Guerin. Heterogeneity, structure, and role in the regulation of cytokine secretion. J Biol Chem 272: 23094-23103.
33. Paget, M.S., Kang, J.G., Roe, J.H., and Buttner, M.J. (1998) SigmaR, 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.
34. Park, J.H., and Roe, J.H. (2008) Mycothiol regulates and is regulated by a thiol-specific antisigma factor RsrA and sigma(R) in Streptomyces coelicolor. Mol Microbiol 68: 861-870.
35. Park, J.H., Cha, C.J., and Roe, J.H. (2006) Identification of genes for mycothiol biosynthesis in Streptomyces coelicolor A3(2). J Microbiol 44: 121-125.
36. Redenbach, M., Kieser, H.M., Denapaite, D., Eichner, A., Cullum, J., Kinashi, H., etal. (1996) A set of ordered cosmids and a detailed genetic and physical map for the 8 Mb Streptomyces coelicolor A3(2) chromosome. Mol Microbiol 21: 77-96.
37. Rigali, S., Nothaft, H., Noens, E.E.E., Schlicht, M., Colson, S., Müller, M., etal. (2006) The sugar phosphotransferase system of Streptomyces coelicolor is regulated by the GntR-family regulator DasR and links N-acetylglucosamine metabolism to the control of development. Mol Microbiol 61: 1237-1251.
38. Rigali, S., Titgemeyer, F., Barends, S., Mulder, S., Thomae, A.W., Hopwood, D.A., etal. (2008) Feast or famine: the global regulator DasR links nutrient stress to antibiotic production by Streptomyces. EMBO Rep 9: 670-675.
39. Rodionov, D.A., Kurnasov, O.V., Stec, B., Wang, Y., Roberts, M.F., and Osterman, A.L. (2007) Genomic identification and in vitro reconstitution of a complete biosynthetic pathway for the osmolyte di-myo-inositol-phosphate. Proc Natl Acad Sci USA 104: 4279-4284.
40. Salman, M., Lonsdale, J.T., Besra, G.S., and Brennan, P.J. (1999) Phosphatidylinositol synthesis in mycobacteria. Biochim Biophys Acta 1436: 437-450.
41. Sambrook, J., and Russell, D.W. (2001) Molecular Cloning: A Laboratory Manual. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
42. Santos, H., and da Costa, M.S. (2002) Compatible solutes of organisms that live in hot saline environments. Environ Microbiol 4: 501-509.
43. Schneider, D., Bruton, C.J., and Chater, K.F. (2000) Duplicated gene clusters suggest an interplay of glycogen and trehalose metabolism during sequential stages of aerial mycelium development in Streptomyces coelicolor A3(2). Mol Gen Genet 263: 543-553.
44. Squire, D.J., Xu, M., Cole, J.A., Busby, S.J., and Browning, D.F. (2009) Competition between NarL-dependent activation and Fis-dependent repression controls expression from the Escherichia coli yeaR and ogt promoters. Biochem J 420: 249-257.
45. Tian, Y., Fowler, K., Findlay, K., Tan, H., and Chater, K.F. (2007) An unusual response regulator influences sporulation at early and late stages in Streptomyces coelicolor. J Bacteriol 189: 2873-2885.
46. Yang, H., Wang, L., Xie, Z., Tian, Y., Liu, G., and Tan, H. (2007) The tyrosine degradation gene hppD is transcriptionally activated by HpdA and repressed by HpdR in Streptomyces coelicolor, while hpdA is negatively autoregulated and repressed by HpdR. Mol Microbiol 65: 1064-1077.
47. Zhang, G., Tian, Y., Hu, K., Feng, C., and Tan, H. (2010) SCO3900, co-transcripted with three downstream genes, is involved in the differentiation of Streptomyces coelicolor. Curr Microbiol 60: 268-273.