Pathway-specific regulation revisited: cross-regulation of multiple disparate gene clusters by PAS-LuxR transcriptional regulators

Applied Microbiology and Biotechnology

Volumn 99, Issue 12, 2015, Pages 5123-5135

  Vicente, Cláudia M ^a,b   Payero, Tamara D ^a,b   Santos Aberturas, Javier ^b,c   Barreales, Eva G ^a   de Pedro, Antonio ^a   Aparicio, Jesús F ^a  

^a UNIVERSITY OF LEÓN   (Spain)

^b Institute of Biotechnology INBIOTEC Parque Científico de León   (Spain)

^c UNIVERSITY OF GREIFSWALD   (Germany)

Author keywords

Gene regulation; LuxR; Metabolic engineering; PAS domain; Polyene macrolide; Regulator binding site; Streptomyces

Indexed keywords

BACTERIA; BINDING ENERGY; BIOCHEMISTRY; BIOMOLECULES; BIOSYNTHESIS; COMPLEX NETWORKS; ELECTROPHORETIC MOBILITY; GENE EXPRESSION; METABOLIC ENGINEERING; METABOLISM; METABOLITES; ORGANIC COMPOUNDS; POLYMERASE CHAIN REACTION; PROCESS CONTROL; PROTEINS; REPAIR; TRANSCRIPTION;

ELECTROPHORETIC MOBILITY SHIFT ASSAY; LUXR; PAS DOMAIN; POLYENE MACROLIDE; QUANTITATIVE POLYMERASE CHAIN REACTION; STREPTOMYCES; TRANSCRIPTIONAL REGULATION; TRANSCRIPTIONAL REGULATOR;

GENES;

OLIGOMYCIN; PAS LUXR TRANSCRIPTIONAL REGULATOR; REGULATOR PROTEIN; UNCLASSIFIED DRUG; BACTERIAL PROTEIN; LUXR AUTOINDUCER BINDING PROTEINS; REPRESSOR PROTEIN; TRANSACTIVATOR PROTEIN;

ANTIMICROBIAL ACTIVITY; BACTERIUM; DIFFERENTIATION; DNA; GENE EXPRESSION; INHIBITOR; METABOLISM; MORPHOLOGY; POLYMERASE CHAIN REACTION; PROTEIN; SECONDARY METABOLITE;

ARTICLE; BINDING SITE; BIOINFORMATICS; COMPUTER MODEL; CONTROLLED STUDY; GEL MOBILITY SHIFT ASSAY; GENE CLUSTER; GENE EXPRESSION; GENETIC COMPLEMENTATION; GENETIC TRANSCRIPTION; GENOME; NONHUMAN; PROMOTER REGION; QUANTITATIVE ANALYSIS; REGULATORY MECHANISM; SECONDARY METABOLISM; STREPTOMYCES AVERMITILIS; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MULTIGENE FAMILY; STREPTOMYCES;

PROTEIDAE; STREPTOMYCES; STREPTOMYCES AVERMITILIS; STREPTOMYCINEAE;

BACTERIAL PROTEINS; GENE EXPRESSION REGULATION, BACTERIAL; MULTIGENE FAMILY; PROMOTER REGIONS, GENETIC; REPRESSOR PROTEINS; STREPTOMYCES; TRANS-ACTIVATORS;

EID: 84929946727     PISSN: 01757598     EISSN: 14320614     Source Type: Journal    
DOI: 10.1007/s00253-015-6472-x     Document Type: Article

References (54)

1. Antón N, Mendes MV, Martín JF, Aparicio JF (2004) Identification of PimR as a positive regulator of pimaricin biosynthesis in Streptomyces natalensis. J Bacteriol 186:2567–2575. doi:10.1128/JB.186.9.2567-2575.2004
2. Antón N, Santos-Aberturas J, Mendes MV, Guerra SM, Martín JF, Aparicio JF (2007) PimM, a PAS domain positive regulator of pimaricin biosynthesis in Streptomyces natalensis. Microbiology 53:3174–3183. doi:10.1099/mic. 0.2007/009126-0
3. Becker NA, Peters JP, Lionberger TA, Maher LJ III (2013) Mechanism of promoter repression by Lac repressor-DNA loops. Nucleic Acids Res 41:156–166. doi:10.1093/nar/gks1011
4. Belitsky BR, Sonenshein AL (1999) An enhancer element located downstream of the major glutamate dehydrogenase gene of Bacillus subtilis. Proc Natl Acad Sci U S A 96:10290–10295. doi:10.1073/pnas.96.18.10290
5. Bellier A, Gominet M, Mazodier P (2006) Post-translational control of the Streptomyces lividans ClgR regulon by ClpP. Microbiology 152:1021–1027. doi:10.1099/mic. 0.28564-0
6. Bi C, Rogan PK (2006) BIPAD: a web server for modeling bipartite sequence elements. BMC Bioinforma 7:76. doi:10.1186/1471-2105-7-76
7. Bourn WR, Babb B (1995) Computer assisted identification and classification of streptomycete promoters. Nucleic Acids Res 23:3696–3703. doi:10.1093/nar/23.18.3696
8. Caffrey P, Aparicio JF, Malpartida F, Zotchev SB (2008) Biosynthetic engineering of polyene macrolides towards generation of improved antifungal and antiparasitic agents. Curr Top Med Chem 8:639–653. doi:10.2174/156802608784221479
9. Cann JR (1998) Theoretical studies on the mobility-shift assay of protein-DNA complexes. Electrophoresis 19:127–141. doi:10.1002/elps.1150190202
10. Challis GL, Hopwood DA (2003) Synergy and contingency as driving forces for the evolution of multiple secondary metabolite production by Streptomyces species. Proc Natl Acad Sci U S A 100:14555–14561. doi:10.1073/pnas.1934677100
11. Chen L, Chen J, Jiang Y, Zhang W, Jiang W, Lu Y (2009) Transcriptomics analyses reveal global roles of the regulator AveI in Streptomyces avermitilis. FEMS Microbiol Lett 298:199–207. doi:10.1111/j.1574-6968.2009.01721.x
12. Cournac A, Plumbridge J (2013) DNA looping in prokaryotes: experimental and theoretical approaches. J Bacteriol 195:1109–1119. doi:10.1128/JB.02038-12
13. Dole S, Nagarajavel V, Schnetz L (2004) The histone-like nucleoid structuring protein H-NS represses the Escherichia coli bgl operon downstream of the promoter. Mol Microbiol 52:589–600. doi:10.1111/j.1365-2958.2004.04001.x
14. Du YL, Chen SF, Cheng LY, Shen XL, Tian Y, Li YQ (2009) Identification of a novel Streptomyces chattanoogensis L10 and enhancing its natamycin production by overexpressing positive regulator ScnRII. J Microbiol 47:506–513. doi:10.1007/s12275-009-0014-0
15. Enríquez LL, Mendes MV, Antón N, Tunca S, Guerra SM, Martín JF, Aparicio JF (2006) An efficient gene transfer system for the pimaricin producer Streptomyces natalensis. FEMS Microbiol Lett 257:312–318. doi:10.1111/j.1574-6968.2006.00189.x
16. Frith MC, Li MC, Weng Z (2003) Cluster-Buster: finding dense clusters of motifs in DNA sequences. Nucleic Acids Res 31:3666–3668. doi:10.1093/nar/gkg540
17. Gao C, Hindra Mulder D, Yin C, Elliot M.A (2012) Crp is a global regulator of antibiotic production in Streptomyces. mBio 3, e00407-12. doi: 10.1128/mBio.00407-12
18. Gordon ND, Ottaviano GL, Connell SE, Tobkin GV, Son CH, Shterental S, Gehring AM (2008) Secreted-protein response to sigmaU activity in Streptomyces coelicolor. J Bacteriol 190:894–904. doi:10.1128/JB.01759-07
19. Guerra SM, Rodríguez-García A, Santos-Aberturas J, Vicente CM, Payero TD, Martín JF, Aparicio JF (2012) LAL regulators SCO0877 and SCO7173 as pleiotropic modulators of phosphate starvation response and actinorhodin biosynthesis in Streptomyces coelicolor. PLoS One 7:e31475. doi:10.1371/journal.pone.0031475
20. Hefti MH, Francoijs K-J, de Vries SC, Dixon R, Vervoort J (2004) The PAS fold. A redefinition of the PAS domain based upon structural prediction. Eur J Biochem 271:1198–1208. doi:10.1111/j.1432-1033.2004.04023.x
21. Higgens CE, Hamill RL, Sands TH, Hoehn MM, Davis NE (1974) The occurrence of deacetoxycephalosporin C in fungi and streptomycetes. J Antibiot 27:298–300
22. Horinouchi S (2003) AfsR as an integrator of signals that are sensed by multiple serine/threonine kinases in Streptomyces coelicolor A3(2). J Ind Microbiol Biotechnol 30:462–467. doi:10.1007/s10295-003-0063-z
23. Huang J, Shi J, Molle V, Sohlberg B, Weaver D, Bibb MJ, Karoonuthaisiri N, Lih CJ, Kao CM, Buttner MJ, Cohen SN (2005) Cross-regulation among disparate antibiotic biosynthetic pathways of Streptomyces coelicolor. Mol Microbiol 58:1276–1287. doi:10.1111/j.1365-2958.2005.04879.x
24. Ikeda H, Shin-ya K, Omura S (2014) Genome mining of the Streptomyces avermitilis genome and development of genome-minimized hosts for heterologous expression of biosynthetic gene clusters. J Ind Microbiol Biotechnol 41:233–250. doi:10.1007/s10295-013-1327-x
25. Kells PM, Ouellet H, Santos-Aberturas J, Aparicio JF, Podust LM (2010) Structure of cytochrome P450 PimD suggests epoxidation of the polyene macrolide pimaricin occurs via a hydroperoxoferric intermediate. Chem Biol 17:841–851. doi:10.1016/j.chembiol.2010.05.026
26. Kieser T, Bibb MJ, Buttner MJ, Chater KF, Hopwood DA (2000) Practical Streptomyces genetics. John Innes Foundation, Norwich
27. Linton KJ, Higgins CF (1998) The Escherichia coli ATP-binding cassette (ABC) proteins. Mol Microbiol 28:5–13. doi:10.1046/j.1365-2958.1998.00764.x
28. Maris AE, Sawaya MR, Kaczor-Grzeskowiak M, Jarvis MR, Bearson SM, Kopka ML, Schröder I, Gunsalus RP, Dickerson RE (2002) Dimerization allows DNA target site recognition by the NarL response regulator. Nat Struct Biol 9:771–778. doi:10.1038/nsb845
29. Martín JF, Aparicio JF (2009) Enzymology of the polyenes pimaricin and candicidin biosynthesis. Methods Enzymol 459:215–242. doi:10.1016/S0076-6879(09)04610-2
30. Mendes MV, Recio E, Fouces R, Luiten R, Martín JF, Aparicio JF (2001) Engineered biosynthesis of novel polyenes: a pimaricin derivative produced by targeted gene disruption in Streptomyces natalensis. Chem Biol 8:635–644. doi:10.1016/S1074-5521(01)00033-3
31. Mendes MV, Antón N, Martín JF, Aparicio JF (2005) Characterization of the polyene macrolid P450 epoxidase from Streptomyces natalensis that converts de-epoxypimaricin into pimaricin. Biochem J 386:57–62. doi:10.1042/BJ20040490
32. Mendes MV, Recio E, Antón N, Guerra SM, Santos-Aberturas J, Martín JF, Aparicio JF (2007) Cholesterol oxidases act as signaling proteins for the biosynthesis of the polyene macrolide pimaricin. Chem Biol 14:279–290. doi:10.1016/j.chembiol.2007.01.010
33. Möglich A, Ayers RA, Moffat K (2009) Structure and signaling mechanism of Per-ARNT-Sim domains. Structure 17:1282–1294. doi:10.1016/j.str.2009.08.011
34. Pfaffl MW (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29:e45. doi:10.1093/nar/29.9.e45
35. Pfaffl MW, Horgan GW, Dempfle L (2002) Relative expression software tool (REST) for group-wise comparison and statistical analysis of relative expression results in real-time PCR. Nucleic Acids Res 30:e36. doi:10.1093/nar/30.9.e36
36. Rasmussen R (2000) Quantification on the LightCycler. In: Meuer S, Wittwer C, Nakagawara K (eds) Rapid Cycle Real-Time PCR, Methods and Applications. Springer Press, Heidelberg, pp 21–34
37. Rocak S, Linder P (2004) DEAD-box proteins: the driving forces behind RNA metabolism. Nat Rev Mol Cell Biol 5:232–241
38. Rozen S, Skaletsky HJ (2000) Primer3 on the WWW for general users and for biologist programmers. In: Krawetz S, Misener S (eds) Bioinformatics methods and protocols: methods in molecular biology. HumanaPress, Totowa, pp 365–386
39. Santos-Aberturas J, Vicente CM, Guerra SM, Payero TD, Martín JF, Aparicio JF (2011a) Molecular control of polyene macrolide biosynthesis: direct binding of the regulator PimM to eight promoters of pimaricin genes and identification of binding boxes. J Biol Chem 286:9150–9161. doi:10.1074/jbc.M110.182428
40. Santos-Aberturas J, Payero TD, Vicente CM, Guerra SM, Cañibano C, Martín JF, Aparicio JF (2011b) Functional conservation of PAS-LuxR transcriptional regulators in polyene macrolide biosynthesis. Metab Eng 13:756–767. doi:10.1016/j.ymben.2011.09.011
41. Santos-Aberturas J, Vicente CM, Payero TD, Martín-Sánchez L, Cañibano C, Martín JF, Aparicio JF (2012) Hierarchical control on polyene macrolide biosynthesis: PimR modulates pimaricin production via the PAS-LuxR transcriptional activator PimM. PLoS One 7:e38536. doi:10.1371/journal.pone.0038536
42. Scheu AK, Martínez E, Soliveri J, Malpartida F (1997) abaB, a putative regulator for secondary metabolism in Streptomyces. FEMS Microbiol Lett 147:29–36. doi:10.1016/S0378-1097(96)00498-3
43. Schneider TD (1997) Information content of individual genetic sequences. J Theor Biol 189:427–441. doi:10.1006/jtbi.1997.0540
44. Schroeder A, Mueller O, Stocker S, Salowsky R, Leiber M, Gassmann M, Lightfoot S, Menzel W, Granzow M, Ragg T (2006) The RIN: an RNA integrity number for assigning integrity values to RNA measurements. BMC Mol Biol 7:3. doi:10.1186/1471-2199-7-3
45. Sekurova ON, Brautaset T, Sletta H, Borgos SEF, Jakobsen OM, Ellingsen TE, Strom AR, Valla S, Zotchev SB (2004) In vivo analysis of the regulatory genes in the nystatin biosynthetic gene cluster of Streptomyces noursei ATCC 11455 reveals their differential control over antibiotic biosynthesis. J Bacteriol 186:1345–1354. doi:10.1128/JB.186.5.1345-1354.2004
46. Staudenmaier H, van Hove B, Yaraghi Z, Braun V (1989) Nucleotide sequences of the fecBCDE genes and locations of the proteins suggest a periplasmic-binding-protein-dependent transport mechanism for iron(III) dicitrate in Escherichia coli. J Bacteriol 171:2626–2633
47. Taylor BL, Zhulin IB (1999) PAS domains: internal sensors of oxygen, redox potential, and light. Microbiol Mol Biol Rev 63:479–506
48. Vannini A, Volpari C, Gargioli C, Muraglia E, Cortese R, de Francesco R, Neddermann P, Marco SD (2002) The crystal structure of the quorum sensing protein TraR bound to its autoinducer and target DNA. EMBO J 21:4393–4401. doi:10.1093/emboj/cdf459
49. Vicente CM, Santos-Aberturas J, Guerra SM, Payero TD, Martín JF, Aparicio JF (2009) PimT, an amino acid exporter controls polyene production via secretion of the quorum sensing pimaricin-inducer PI-factor in Streptomyces natalensis. Microb. Cell Fact.8, 33. doi: 10.1186/1475-2859-8-33
50. Vicente CM, Santos-Aberturas J, Payero TD, Barreales EG, de Pedro A, Aparicio JF (2014) PAS-LuxR transcriptional control of filipin biosynthesis in S. avermitilis. Appl Microbiol Biotechnol 98:9311–9324. doi:10.1007/s00253-014-5998-7
51. Wei J, Meng X, Wang Q (2011) Enhanced production of aureofuscin by over-expression of AURJ3M, positive regulator of aureofuscin biosynthesis in Streptomyces aureofuscus. Lett Appl Microbiol 47:506–513. doi:10.1111/j.1472-765X.2011.03003.x
52. Wisedchaisri G, Wu M, Rice AE, Roberts DM, Sherman DR, Hol WG (2005) Structures of Mycobacterium tuberculosis DosR and DosR-DNA complex involved in gene activation during adaptation to hypoxic latency. J Mol Biol 354:630–641. doi:10.1016/j.jmb.2005.09.048
53. Yao J, Rock CO (2013) Phosphatidic acid synthesis in bacteria. Biochim Biophys Acta 1831:495–502. doi:10.1016/j.bbalip.2012.08.018
54. Yu Q, Bai L, Zhou X, Deng Z (2012) Inactivation of the positive LuxR-type oligomycin biosynthesis regulators OlmRI and OlmRII increases avermectin production in Streptomyces avermitilis. Chin Sci Bull 57:869–876. doi:10.1007/s11434-011-4865-5