Two-component systems in Streptomyces: Key regulators of antibiotic complex pathways

Microbial Cell Factories

Volumn 12, Issue 1, 2013, Pages

  Rodríguez, Héctor ^a   Rico, Sergio ^a   Díaz, Margarita ^a   Santamaría, Ramón I ^a  

^a Instituto de Biología Funcional y Genómica and Departamento de Microbiología y Genética   (Spain)

Author keywords

Antibiotic production; Secondary metabolism; Streptomyces; Two component systems

Indexed keywords

ANTIBIOTIC AGENT; NITROGEN; PHOSPHATE; UNCLASSIFIED DRUG; UNDECYLPRODIGININE;

ANTIBIOTIC BIOSYNTHESIS; BACTERIAL PHENOMENA AND FUNCTIONS; DRUG MANUFACTURE; GENETIC ENGINEERING; GROWTH CURVE; METABOLITE; NITROGEN AVAILABILITY; NONHUMAN; PRODUCTIVITY; REVIEW; SIGNAL TRANSDUCTION; STREPTOMYCES; STREPTOMYCES COELICOLOR; TWO COMPONENT SYSTEM;

STREPTOMYCES;

ANTI-BACTERIAL AGENTS; SECONDARY METABOLISM; STREPTOMYCES;

EID: 84890322298     PISSN: None     EISSN: 14752859     Source Type: Journal    
DOI: 10.1186/1475-2859-12-127     Document Type: Review

References (76)

1. Hopwood DA. Streptomyces in Nature and Medicine. The Antibiotic Makers 2007, New York: Oxford University Press Inc.
2. Krell T, Lacal J, Busch A, Silva-Jimenez H, Guazzaroni ME, Ramos JL. Bacterial sensor kinases: diversity in the recognition of environmental signals. Annu Rev Microbiol 2010, 64:539-559. 10.1146/annurev.micro.112408.134054, 20825354.
3. Stock AM, Robinson VL, Goudreau PN. Two-component signal transduction. Annu Rev Biochem 2000, 69:183-215. 10.1146/annurev.biochem.69.1.183, 10966457.
4. Mascher T, Helmann JD, Unden G. Stimulus perception in bacterial signal-transducing histidine kinases. Microbiol Mol Biol Rev 2006, 70:910-938. 10.1128/MMBR.00020-06, 1698512, 17158704.
5. Bentley SD, Chater KF, Cerdeño-Tárraga AM, Challis GL, Thomson NR, James KD, Harris DE, Quail MA, Kieser H, Harper D, et al. Complete genome sequence of the model actinomycete Streptomyces coelicolor A3(2). Nature 2002, 417:141-147. 10.1038/417141a, 12000953.
6. Hutchings MI, Hoskisson PA, Chandra G, Buttner MJ. Sensing and responding to diverse extracellular signals. Analysis of the sensor kinases and response regulators of Streptomyces coelicolor A3(2). Microbiology 2004, 150:2795-2806. 10.1099/mic.0.27181-0, 15347739.
7. Omura S. The expanded horizon for microbial metabolites-a review. Gene 1992, 115:141-149. 10.1016/0378-1119(92)90552-Z, 1612429.
8. Berdy J. Bioactive microbial metabolites. J Antibiot (Tokyo) 2005, 58:1-26. 10.1038/ja.2005.1, 15813176.
9. Berdy J. Thoughts and facts about antibiotics: where we are now and where we are heading. J Antibiot (Tokyo) 2012, 65:385-395. 10.1038/ja.2012.27, 22511224.
10. Papagianni M. Recent advances in engineering the central carbon metabolism of industrially important bacteria. Microb Cell Fact 2012, 11:50. 10.1186/1475-2859-11-50, 3461431, 22545791.
11. Gomez-Escribano J, Song L, Fox DJ, Yeo V, Bibb MJ, Challis G. Structure and biosynthesis of the unusual polyketide alkaloid coelimycin P1, a metabolic product of the cpk gene cluster of Streptomyces coelicolor M145. Chem Sci 2012, 3:2716-2720.
12. Gottelt M, Kol S, Gomez-Escribano JP, Bibb M, Takano E. Deletion of a regulatory gene within the cpk gene cluster reveals novel antibacterial activity in Streptomyces coelicolor A3(2). Microbiology 2010, 156:2343-2353. 10.1099/mic.0.038281-0, 20447997.
13. Craney A, Ahmed S, Nodwell J. Towards a new science of secondary metabolism. J Antibiot (Tokyo) 2013, 66:387-400. 10.1038/ja.2013.25, 23612726.
14. Sidebottom AM, Johnson AR, Karty JA, Trader DJ, Carlson EE. Integrated metabolomics approach facilitates discovery of an unpredicted natural product suite from Streptomyces coelicolor M145. ACS Chem Biol 2013, 8:2009-2016. 10.1021/cb4002798, 23777274.
15. Martin JF, Liras P. Engineering of regulatory cascades and networks controlling antibiotic biosynthesis in Streptomyces. Curr Opin Microbiol 2010, 13:263-273. 10.1016/j.mib.2010.02.008, 20303823.
16. van Wezel GP, McDowall KJ. The regulation of the secondary metabolism of Streptomyces: new links and experimental advances. Nat Prod Rep 2011, 28:1311-1333. 10.1039/c1np00003a, 21611665.
17. Huang J, Shi J, Molle V, Sohlberg B, Weaver D, Bibb MJ, Karoonuthaisiri N, Lih CJ, Kao CM, Buttner MJ, Cohen SN. Cross-regulation among disparate antibiotic biosynthetic pathways of Streptomyces coelicolor. Mol Microbiol 2005, 58:1276-1287. 10.1111/j.1365-2958.2005.04879.x, 16313616.
18. Arias P, Fernandez-Moreno MA, Malpartida F. Characterization of the pathway-specific positive transcriptional regulator for actinorhodin biosynthesis in Streptomyces coelicolor A3(2) as a DNA-binding protein. J Bacteriol 1999, 181:6958-6968. 94170, 10559161.
19. Takano E, Gramajo HC, Strauch E, Andres N, White J, Bibb MJ. Transcriptional regulation of the redD transcriptional activator gene accounts for growth-phase-dependent production of the antibiotic undecylprodigiosin in Streptomyces coelicolor A3(2). Mol Microbiol 1992, 6:2797-2804. 10.1111/j.1365-2958.1992.tb01459.x, 1435258.
20. White J, Bibb M. bldA dependence of undecylprodigiosin production in Streptomyces coelicolor A3(2) involves a pathway-specific regulatory cascade. J Bacteriol 1997, 179:627-633. 178740, 9006013.
21. Takano E, Kinoshita H, Mersinias V, Bucca G, Hotchkiss G, Nihira T, Smith CP, Bibb M, Wohlleben W, Chater K. A bacterial hormone (the SCB1) directly controls the expression of a pathway-specific regulatory gene in the cryptic type I polyketide biosynthetic gene cluster of Streptomyces coelicolor. Mol Microbiol 2005, 56:465-479. 10.1111/j.1365-2958.2005.04543.x, 15813737.
22. Ryding NJ, Anderson TB, Champness WC. Regulation of the Streptomyces coelicolor calcium-dependent antibiotic by absA, encoding a cluster-linked two-component system. J Bacteriol 2002, 184:794-805. 10.1128/JB.184.3.794-805.2002, 139508, 11790750.
23. Wang R, Mast Y, Wang J, Zhang W, Zhao G, Wohlleben W, Lu Y, Jiang W. Identification of two-component system AfsQ1/Q2 regulon and its cross-regulation with GlnR in Streptomyces coelicolor. Mol Microbiol 2013, 87:30-48. 10.1111/mmi.12080, 23106203.
24. Yu Z, Zhu H, Dang F, Zhang W, Qin Z, Yang S, Tan H, Lu Y, Jiang W. Differential regulation of antibiotic biosynthesis by DraR-K, a novel two-component system in Streptomyces coelicolor. Mol Microbiol 2012, 85:535-556. 10.1111/j.1365-2958.2012.08126.x, 22676800.
25. Bibb MJ. Regulation of secondary metabolism in streptomycetes. Curr Opin Microbiol 2005, 8:208-215. 10.1016/j.mib.2005.02.016, 15802254.
26. Liu G, Chater KF, Chandra G, Niu G, Tan H. Molecular regulation of antibiotic biosynthesis in Streptomyces. Microbiol Mol Biol Rev 2013, 77:112-143. 10.1128/MMBR.00054-12, 23471619.
27. Martin JF, Liras P. Cascades and networks of regulatory genes that control antibiotic biosynthesis. Subcell Biochem 2012, 64:115-138. 10.1007/978-94-007-5055-5_6, 23080248.
28. Sanchez S, Chavez A, Forero A, Garcia-Huante Y, Romero A, Sanchez M, Rocha D, Sanchez B, Avalos M, Guzman-Trampe S, et al. Carbon source regulation of antibiotic production. J Antibiot (Tokyo) 2010, 63:442-459. 10.1038/ja.2010.78, 20664603.
29. Martín JF, Sola-Landa A, Rodriguez-Garcia A. Two component Systems in Streptomyces. Two-component Systems in Bacteria 2012, Caister Academic Press, Gross R, Beier D.
30. Ishizuka H, Horinouchi S, Kieser HM, Hopwood DA, Beppu T. A putative two-component regulatory system involved in secondary metabolism in Streptomyces spp. J Bacteriol 1992, 174:7585-7594. 207469, 1339426.
31. Shu D, Chen L, Wang W, Yu Z, Ren C, Zhang W, Yang S, Lu Y, Jiang W. afsQ1-Q2-sigQ is a pleiotropic but conditionally required signal transduction system for both secondary metabolism and morphological development in Streptomyces coelicolor. Appl Microbiol Biotechnol 2009, 81:1149-1160. 10.1007/s00253-008-1738-1, 18949475.
32. Martin JF, Sola-Landa A, Santos-Beneit F, Fernandez-Martinez LT, Prieto C, Rodriguez-Garcia A. Cross-talk of global nutritional regulators in the control of primary and secondary metabolism in Streptomyces. Microb Biotechnol 2011, 4:165-174. 10.1111/j.1751-7915.2010.00235.x, 21342462.
33. Yeo KJ, Kim EH, Hwang E, Han YH, Eo Y, Kim HJ, Kwon O, Hong YS, Cheong C, Cheong HK. pH-dependent structural change of the extracellular sensor domain of the DraK histidine kinase from Streptomyces coelicolor. Biochem Biophys Res Commun 2013, 431:554-559. 10.1016/j.bbrc.2013.01.018, 23321311.
34. Yeo KJ, Han YH, Eo Y, Cheong HK. Expression, purification, crystallization and preliminary X-ray analysis of the extracellular sensory domain of DraK histidine kinase from Streptomyces coelicolor. Acta Crystallogr Sect F: Struct Biol Cryst Commun 2013, 69:909-911. 10.1107/S1744309113018769, 23908041.
35. Apel AK, Sola-Landa A, Rodriguez-Garcia A, Martin JF. Phosphate control of phoA, phoC and phoD gene expression in Streptomyces coelicolor reveals significant differences in binding of PhoP to their promoter regions. Microbiology 2007, 153:3527-3537. 10.1099/mic.0.2007/007070-0, 17906150.
36. Martin JF. Phosphate control of the biosynthesis of antibiotics and other secondary metabolites is mediated by the PhoR-PhoP system: an unfinished story. J Bacteriol 2004, 186:5197-5201. 10.1128/JB.186.16.5197-5201.2004, 490900, 15292120.
37. Hulett FM. The signal-transduction network for Pho regulation in Bacillus subtilis. Mol Microbiol 1996, 19:933-939. 10.1046/j.1365-2958.1996.421953.x, 8830274.
38. Pragai Z, Harwood CR. Regulatory interactions between the Pho and sigma(B)-dependent general stress regulons of Bacillus subtilis. Microbiology 2002, 148:1593-1602.
39. Torriani-Gorini A, Yagil E, Silver S. Phosphate in Microorganisms. Am Soc Microbiol 1994, Washington, D. C.
40. Sola-Landa A, Moura RS, Martin JF. The two-component PhoR-PhoP system controls both primary metabolism and secondary metabolite biosynthesis in Streptomyces lividans. Proc Natl Acad Sci USA 2003, 100:6133-6138. 10.1073/pnas.0931429100, 156338, 12730372.
41. Santos-Beneit F, Rodriguez-Garcia A, Sola-Landa A, Martin JF. Cross-talk between two global regulators in Streptomyces: PhoP and AfsR interact in the control of afsS, pstS and phoRP transcription. Mol Microbiol 2009, 72:53-68. 10.1111/j.1365-2958.2009.06624.x, 19220751.
42. Allenby NE, Laing E, Bucca G, Kierzek AM, Smith CP. Diverse control of metabolism and other cellular processes in Streptomyces coelicolor by the PhoP transcription factor: genome-wide identification of in vivo targets. Nucleic Acids Res 2012, 40:9543-9556. 10.1093/nar/gks766, 3479208, 22904076.
43. Sola-Landa A, Rodriguez-Garcia A, Franco-Dominguez E, Martin JF. Binding of PhoP to promoters of phosphate-regulated genes in Streptomyces coelicolor: identification of PHO boxes. Mol Microbiol 2005, 56:1373-1385. 10.1111/j.1365-2958.2005.04631.x, 15882427.
44. Horinouchi S. AfsR as an integrator of signals that are sensed by multiple serine/threonine kinases in Streptomyces coelicolor A3(2). J Ind Microbiol Biotechnol 2003, 30:462-467. 10.1007/s10295-003-0063-z, 12884127.
45. Lee PC, Umeyama T, Horinouchi S. afsS is a target of AfsR, a transcriptional factor with ATPase activity that globally controls secondary metabolism in Streptomyces coelicolor A3(2). Mol Microbiol 2002, 43:1413-1430. 10.1046/j.1365-2958.2002.02840.x, 11952895.
46. Santos-Beneit F, Barriuso-Iglesias M, Fernandez-Martinez LT, Martinez-Castro M, Sola-Landa A, Rodriguez-Garcia A, Martin JF. The RNA polymerase omega factor RpoZ is regulated by PhoP and has an important role in antibiotic biosynthesis and morphological differentiation in Streptomyces coelicolor. Appl Environ Microbiol 2011, 77:7586-7594. 10.1128/AEM.00465-11, 3209170, 21908625.
47. Tseng HC, Chen CW. A cloned ompR-like gene of Streptomyces lividans 66 suppresses defective melC1, a putative copper-transfer gene. Mol Microbiol 1991, 5:1187-1196. 10.1111/j.1365-2958.1991.tb01892.x, 1956295.
48. Chang HM, Chen MY, Shieh YT, Bibb MJ, Chen CW. The cutRS signal transduction system of Streptomyces lividans represses the biosynthesis of the polyketide antibiotic actinorhodin. Mol Microbiol 1996, 21:1075-1085.
49. Wang W, Shu D, Chen L, Jiang W, Lu Y. Cross-talk between an orphan response regulator and a noncognate histidine kinase in Streptomyces coelicolor. FEMS Microbiol Lett 2009, 294:150-156. 10.1111/j.1574-6968.2009.01563.x, 19341396.
50. Li YQ, Chen PL, Chen SF, Wu D, Zheng J. A pair of two-component regulatory genes ecrA1/A2 in S. coelicolor. J Zhejiang Univ (Sci) 2004, 5:173-179. 10.1631/jzus.2004.0173, 14674028.
51. Wang C, Ge H, Dong H, Zhu C, Li Y, Zheng J, Cen P. A novel pair of two-component signal transduction system ecrE1/ecrE2 regulating antibiotic biosynthesis in Streptomyces coelicolor. Biologia 2007, 62:511-516.
52. Brian P, Riggle PJ, Santos RA, Champness WC. Global negative regulation of Streptomyces coelicolor antibiotic synthesis mediated by an absA-encoded putative signal transduction system. J Bacteriol 1996, 178:3221-3231. 178074, 8655502.
53. Anderson T, Brian P, Riggle P, Kong R, Champness W. Genetic suppression analysis of non-antibiotic-producing mutants of the Streptomyces coelicolor absA locus. Microbiology 1999, 145(Pt 9):2343-2353.
54. Sheeler NL, MacMillan SV, Nodwell JR. Biochemical activities of the absA two-component system of Streptomyces coelicolor. J Bacteriol 2005, 187:687-696. 10.1128/JB.187.2.687-696.2005, 543558, 15629939.
55. Anderson TB, Brian P, Champness WC. Genetic and transcriptional analysis of absA, an antibiotic gene cluster-linked two-component system that regulates multiple antibiotics in Streptomyces coelicolor. Mol Microbiol 2001, 39:553-566. 10.1046/j.1365-2958.2001.02240.x, 11169098.
56. McKenzie NL, Nodwell JR. Phosphorylated AbsA2 negatively regulates antibiotic production in Streptomyces coelicolor through interactions with pathway-specific regulatory gene promoters. J Bacteriol 2007, 189:5284-5292. 10.1128/JB.00305-07, 1951880, 17513473.
57. McKenzie NL, Nodwell JR. Transmembrane topology of the AbsA1 sensor kinase of Streptomyces coelicolor. Microbiology 2009, 155:1812-1818. 10.1099/mic.0.028431-0, 19389775.
58. Lu Y, Wang W, Shu D, Zhang W, Chen L, Qin Z, Yang S, Jiang W. Characterization of a novel two-component regulatory system involved in the regulation of both actinorhodin and a type I polyketide in Streptomyces coelicolor. Appl Microbiol Biotechnol 2007, 77:625-635. 10.1007/s00253-007-1184-5, 17899070.
59. Yepes A, Rico S, Rodriguez-Garcia A, Santamaria RI, Diaz M. Novel two-component systems implied in antibiotic production in Streptomyces coelicolor. PLoS One 2011, 6:e19980. 10.1371/journal.pone.0019980, 3098853, 21625497.
60. Mader U, Antelmann H, Buder T, Dahl MK, Hecker M, Homuth G. Bacillus subtilis functional genomics: genome-wide analysis of the DegS-DegU regulon by transcriptomics and proteomics. Mol Genet Genomics 2002, 268:455-467. 10.1007/s00438-002-0774-2, 12471443.
61. Ogura M, Yamaguchi H, Yoshida K, Fujita Y, Tanaka T. DNA microarray analysis of Bacillus subtilis DegU, ComA and PhoP regulons: an approach to comprehensive analysis of B.subtilis two-component regulatory systems. Nucleic Acids Res 2001, 29:3804-3813. 10.1093/nar/29.18.3804, 55910, 11557812.
62. Rozas D, Gullon S, Mellado RP. A novel two-component system involved in the transition to secondary metabolism in Streptomyces coelicolor. PLoS One 2012, 7:e31760. 10.1371/journal.pone.0031760, 3276577, 22347508.
63. Medema MH, Breitling R, Bovenberg R, Takano E. Exploiting plug-and-play synthetic biology for drug discovery and production in microorganisms. Nat Rev Microbiol 2011, 9:131-137. 10.1038/nrmicro2478, 21189477.
64. Zerikly M, Challis GL. Strategies for the discovery of new natural products by genome mining. Chembiochem 2009, 10:625-633. 10.1002/cbic.200800389, 19165837.
65. Lombo F, Braña AF, Salas JA, Mendez C. Genetic organization of the biosynthetic gene cluster for the antitumor angucycline oviedomycin in Streptomyces antibioticus ATCC 11891. Chembiochem 2004, 5:1181-1187. 10.1002/cbic.200400073, 15368568.
66. Mendez C, Kunzel E, Lipata F, Lombo F, Cotham W, Walla M, Bearden DW, Brana AF, Salas JA, Rohr J. Oviedomycin, an unusual angucyclinone encoded by genes of the oleandomycin-producer Streptomyces antibioticus ATCC11891. J Nat Prod 2002, 65:779-782. 10.1021/np010555n, 12027768.
67. Walsh CT. Combinatorial biosynthesis of antibiotics: challenges and opportunities. Chembiochem 2002, 3:125-134.
68. Gao C, Hindra, Mulder D, Yin C, Elliot MA. Crp is a global regulator of antibiotic production in Streptomyces. MBio 2012, 3:e00407-12. 3520106, 23232715.
69. Laureti L, Song L, Huang S, Corre C, Leblond P, Challis GL, Aigle B. Identification of a bioactive 51-membered macrolide complex by activation of a silent polyketide synthase in Streptomyces ambofaciens. Proc Natl Acad Sci USA 2011, 108:6258-6263. 10.1073/pnas.1019077108, 3076887, 21444795.
70. McKenzie NL, Thaker M, Koteva K, Hughes DW, Wright GD, Nodwell JR. Induction of antimicrobial activities in heterologous streptomycetes using alleles of the Streptomyces coelicolor gene absA1. J Antibiot (Tokyo) 2010, 63:177-182. 10.1038/ja.2010.13, 20224601.
71. Sidda JD, Corre C. Gamma-butyrolactone and furan signaling systems in Streptomyces. Methods Enzymol 2012, 517:71-87.
72. Barakat M, Ortet P, Jourlin-Castelli C, Ansaldi M, Mejean V, Whitworth DE. P2CS: a two-component system resource for prokaryotic signal transduction research. BMC Genomics 2009, 10:315. 10.1186/1471-2164-10-315, 2716373, 19604365.
73. Barakat M, Ortet P, Whitworth DE. P2CS: a database of prokaryotic two-component systems. Nucleic Acids Res 2011, 39:D771-776. 10.1093/nar/gkq1023, 3013651, 21051349.
74. Claros MG, von Heijne G. TopPred II: an improved software for membrane protein structure predictions. Comput Appl Biosci 1994, 10:685-686.
75. von Heijne G. Membrane protein structure prediction. Hydrophobicity analysis and the positive-inside rule. J Mol Biol 1992, 225:487-494. 10.1016/0022-2836(92)90934-C, 1593632.
76. Punta M, Coggill PC, Eberhardt RY, Mistry J, Tate J, Boursnell C, Pang N, Forslund K, Ceric G, Clements J, et al. The Pfam protein families database. Nucleic Acids Res 2012, 40:D290-301. 10.1093/nar/gkr1065, 3245129, 22127870.