Transcriptome-guided identification of SprA as a pleiotropic regulator in Streptomyces chattanoogensis

Applied Microbiology and Biotechnology

Volumn 99, Issue 3, 2015, Pages 1287-1298

  Zhou, Zhen Xing ^a   Xu, Qing Qing ^a   Bu, Qing Ting ^a   Liu, Shui Ping ^a   Yu, Pin ^a   Li, Yong Quan ^a,b  

^a ZHEJIANG UNIVERSITY   (China)

^b Key Laboratory of Microbial Biochemistry and Metabolism Engineering of Zhejiang Province   (China)

Author keywords

GBL receptor; Morphogenesis; Secondary metabolism; Streptomyces

Indexed keywords

BIOCHEMISTRY; BIOSYNTHESIS; ELECTROPHORETIC MOBILITY; ENCODING (SYMBOLS); ESCHERICHIA COLI;

BUTYROLACTONES; ELECTROPHORETIC MOBILITY SHIFT ASSAY; GBL RECEPTOR; MORPHOGENESIS; QUORUM-SENSING; SECONDARY METABOLISM; STREPTOMYCES; TRANSCRIPTOME ANALYSIS;

METABOLISM;

AGAR; FUNGAL PROTEIN; GAMMA BUTYROLACTONE; NATAMYCIN; SCGA PROTEIN; SPRA PROTEIN; TRANSCRIPTOME; UNCLASSIFIED DRUG; BACTERIAL PROTEIN; REPRESSOR PROTEIN;

ARTICLE; BIOSYNTHESIS; CONTROLLED STUDY; DNA FOOTPRINTING; ESCHERICHIA COLI; GEL MOBILITY SHIFT ASSAY; GENE EXPRESSION; GENE SEQUENCE; LIQUID CULTURE; MORPHOGENESIS; MUTANT; NONHUMAN; PLEIOTROPY; STREPTOMYCES; STREPTOMYCES CHATTANOOGENSIS; AMINO ACID SEQUENCE; CHEMISTRY; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MOLECULAR GENETICS; SEQUENCE ALIGNMENT;

4-BUTYROLACTONE; AMINO ACID SEQUENCE; BACTERIAL PROTEINS; GENE EXPRESSION REGULATION, BACTERIAL; MOLECULAR SEQUENCE DATA; REPRESSOR PROTEINS; SEQUENCE ALIGNMENT; STREPTOMYCES; TRANSCRIPTOME;

EID: 84925488983     PISSN: 01757598     EISSN: 14320614     Source Type: Journal    
DOI: 10.1007/s00253-014-6132-6     Document Type: Article

References (35)

1. Ahn SK, Tahlan K, Yu Z, Nodwell J (2007) Investigation of transcription repression and small-molecule responsiveness by TetR-like transcription factors using a heterologous Escherichia coli-based assay. J Bacteriol 189(18):6655–6664. doi:10.1128/Jb.00717-07
2. Bailey TL, Boden M, Buske FA, Frith M, Grant CE, Clementi L, Ren JY, Li WW, Noble WS (2009) MEME SUITE: tools for motif discovery and searching. Nucleic Acids Res 37:W202–W208. doi:10.1093/Nar/Gkp335
3. Baltz RH (1998) Genetic manipulation of antibiotic-producing Streptomyces. Trends Microbiol 6(2):76–83. doi:10.1016/S0966-842x(97)01161-X
4. Bjarnason J, Southward CM, Surette MG (2003) Genomic profiling of iron-responsive genes in Salmonella enterica serovar typhimurium by high-throughput screening of a random promoter library. J Bacteriol 185(16):4973–4982. doi:10.1128/Jb.185.16.4973-4982.2003
5. Bralley P, Jones GH (2003) Overexpression of the polynucleotide phosphorylase gene (pnp) of Streptomyces antibioticus affects mRNA stability and poly(A) tail length but not ppGpp levels. Microbiol-SGM 149:2173–2182. doi:10.1099/mic.0.26334-0
6. Czajkowski R, Jafra S (2009) Quenching of acyl-homoserine lactone-dependent quorum sensing by enzymatic disruption of signal molecules. Acta Biochim Pol 56(1):1–16
7. Delves-Broughton J, Thomas LV, Williams G (2006) Natamycin as an antimycotic preservative on cheese and fermented sausages. Food Aust 58(1–2):19–21
8. 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(4):506–513. doi:10.1007/s12275-009-0014-0
9. ch is required for natamycin biosynthesis and morphological differentiation in Streptomyces chattanoogensis. Microbiol-SGM 157:1300–1311. doi:10.1099/Mic.0.046607-0
10. Du YL, Shen XL, Yu P, Bai LQ, Li YQ (2011b) γ-butyrolactone regulatory system of Streptomyces chattanoogensis links nutrient utilization, metabolism, and development. Appl Environ Microb 77(23):8415–8426. doi:10.1128/Aem.05898-11
11. Edgar R, Domrachev M, Lash AE (2002) Gene Expression Omnibus: NCBI gene expression and hybridization array data repository. Nucleic Acids Res 30(1):207–210. doi:10.1093/Nar/30.1.207
12. Gottelt M, Hesketh A, Bunet R, Puri P, Takano E (2012) Characterisation of a natural variant of the γ-butyrolactone signalling receptor. BMC Res Notes 5:379. doi:10.1186/1756-0500-5-379
13. Gust B, Chandra G, Jakimowicz D, Tian YQ, Bruton CJ, Chater KF (2004) λ red-mediated genetic manipulation of antibiotic-producing Streptomyces. Adv Appl Microbiol 54:107–128. doi:10.1016/S0065-2164(04)54004-2
14. Horinouchi S (2002) A microbial hormone, A-factor, as a master switch for morphological differentiation and secondary metabolism in Streptomyces griseus. Front Biosci 7:D2045–D2057. doi:10.2741/Horinouc
15. Hsiao NH, Nakayama S, Merlo ME, de Vries M, Bunet R, Kitani S, Nihira T, Takano E (2009) Analysis of two additional signaling molecules in Streptomyces coelicolor and the development of a butyrolactone-specific reporter system. Chem Biol 16(9):951–960. doi:10.1016/j.chembiol.2009.08.010
16. Kato JY, Miyahisa I, Mashiko M, Ohnishi Y, Horinouchi S (2004) A single target is sufficient to account for the biological effects of the A-factor receptor protein of Streptomyces griseus. J Bacteriol 186(7):2206–2211. doi:10.1128/Jb.186.7.2203-2211.2004
17. Kieser T, Bibb M, Buttner M, Chater K, Hopwood D (2000) Practical Streptomyces genetics. The John Innes Foundation, Norwich, UK
18. Kinoshita H, Tsuji T, Ipposhi H, Nihira T, Yamada Y (1999) Characterization of binding sequences for butyrolactone autoregulator receptors in streptomycetes. J Bacteriol 181(16):5075–5080
19. Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG (2007) Clustal W and clustal X version 2.0. Bioinformatics 23(21):2947–2948. doi:10.1093/bioinformatics/btm404
20. Liu G, Chater KF, Chandra G, Niu GQ, Tan HR (2013) Molecular regulation of antibiotic biosynthesis in Streptomyces. Microbiol Mol Biol Rev 77(1):112–143. doi:10.1128/Mmbr.00054-12
21. Matsuno K, Yamada Y, Lee CK, Nihira T (2004) Identification by gene deletion analysis of barB as a negative regulator controlling an early process of virginiamycin biosynthesis in Streptomyces virginiae. Arch Microbiol 181(1):52–59. doi:10.1007/s00203-003-0625-5
22. Mehra S, Charaniya S, Takano E, Hu WS (2008) A bistable gene switch for antibiotic biosynthesis: the butyrolactone regulon in Streptomyces coelicolor. PLoS ONE 3(7):e2724. doi:10.1371/Journal.Pone.0002724
23. Nakano H, Takehara E, Nihira T, Yamada Y (1998) Gene replacement analysis of the Streptomyces virginiae barA gene encoding the butyrolactone autoregulator receptor reveals that BarA acts as a repressor in virginiamycin biosynthesis. J Bacteriol 180(13):3317–3322
24. Natsume R, Ohnishi Y, Senda T, Horinouchi S (2004) Crystal structure of a γ-butyrolactone autoregulator receptor protein in Streptomyces coelicolor A3(2). J Mol Biol 336(2):409–19
25. Nishida H, Ohnishi Y, Beppu T, Horinouchi S (2007) Evolution of γ-butyrolactone synthases and receptors in Streptomyces. Environ Microbiol 9(8):1986–1994. doi:10.1111/j.1462-2920.2007.01314.x
26. Ohnishi Y, Yamazaki H, Kato JY, Tomono A, 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 Biotech Bioch 69(3):431–439. doi:10.1271/Bbb.69.431
27. Rigali S, Titgemeyer F, Barends S, Mulder S, Thomae AW, Hopwood DA, van Wezel GP (2008) Feast or famine: the global regulator DasR links nutrient stress to antibiotic production by Streptomyces. EMBO Rep 9(7):670–675. doi:10.1038/embor.2008.83
28. Rioseras B, Lopez-Garcia MT, Yague P, Sanchez J, Manteca A (2014) Mycelium differentiation and development of Streptomyces coelicolor in lab-scale bioreactors: programmed cell death, differentiation, and lysis are closely linked to undecylprodigiosin and actinorhodin production. Bioresour Technol 151:191–198. doi:10.1016/j.biortech.2013.10.068
29. Takano E, Chakraburtty R, Nihira T, Yamada Y, Bibb MJ (2001) A complex role for the γ-butyrolactone SCB1 in regulating antibiotic production in Streptomyces coelicolor A3(2). Mol Microbiol 41(5):1015–1028. doi:10.1046/j.1365-2958.2001.02562.x
30. Takano E, Tao M, Long F, Bibb MJ, Wang L, Li W, Buttner MJ, Bibb MJ, Deng ZX, Chater KF (2003) A rare leucine codon in adpA is implicated in the morphological defect of bldA mutants of Streptomyces coelicolor. Mol Microbiol 50(2):475–486. doi:10.1046/j.1365-2958.2003.3728.x
31. Xu DL, Seghezzi N, Esnault C, Virolle MJ (2010a) Repression of antibiotic production and sporulation in Streptomyces coelicolor by overexpression of a TetR family transcriptional regulator. Appl Environ Microbiol 76(23):7741–7753. doi:10.1128/Aem.00819-10
32. Xu GM, Wang JA, Wang LQ, Tian XY, Yang HH, Fan KQ, Yang KQ, Tan HR (2010b) "Pseudo" γ-Butyrolactone receptors respond to antibiotic signals to coordinate antibiotic biosynthesis. J Biol Chem 285(35):27440–27448. doi:10.1074/jbc.M110.143081
33. Yamada Y, Sugamura K, Kondo K, Yanagimoto M, Okada H (1987) The Structure of Inducing Factors for virginiamycin production in Streptomyces virginiae. J Antibiot 40(4):496–504
34. Yang YH, Song E, Kim EJ, Lee K, Kim WS, Park SS, Hahn JS, Kim BG (2009) NdgR, an IclR-like regulator involved in amino-acid-dependent growth, quorum sensing, and antibiotic production in Streptomyces coelicolor. Appl Microbiol Biotechnol 82(3):501–511. doi:10.1007/s00253-008-1802-x
35. Yang YH, Song E, Kim JN, Lee BR, Kim EJ, Park SH, Kim WS, Park HY, Jeon JM, Rajesh T, Kim YG, Kim BG (2012) Characterization of a new ScbR-like γ-butyrolactone binding regulator (SlbR) in Streptomyces coelicolor. Appl Microbiol Biotechnol 96(1):113–121. doi:10.1007/s00253-011-3803-4