An extracytoplasmic function sigma factor, σ25, differentially regulates avermectin and oligomycin biosynthesis in Streptomyces avermitilis

Applied Microbiology and Biotechnology

Volumn 98, Issue 16, 2014, Pages 7097-7112

  Luo, Shuai ^a   Sun, Di ^a   Zhu, Jianya ^a   Chen, Zhi ^a   Wen, Ying ^a   Li, Jilun ^a  

^a CHINA AGRICULTURAL UNIVERSITY   (China)

Author keywords

Avermectin; ECF factor; Streptomyces avermitilis

Indexed keywords

BACTERIA; BIOCHEMISTRY; BIOSYNTHESIS; GENES; PLANTS (BOTANY); SIGNAL TRANSDUCTION;

ANTIBIOTIC BIOSYNTHESIS; ANTIBIOTIC PRODUCTION; AVERMECTINS; DIRECT REPEAT SEQUENCES; EXTRACYTOPLASMIC FUNCTION; EXTRACYTOPLASMIC FUNCTION SIGMA FACTORS; SIGNAL TRANSDUCTION SYSTEM; STREPTOMYCES AVERMITILIS;

TRANSCRIPTION;

AVERMECTIN; COMPLEMENTARY DNA; GENOMIC DNA; OLIGOMYCIN; RNA POLYMERASE; SIGMA FACTOR;

ANTIBIOTICS; ENZYME ACTIVITY; GENE EXPRESSION; MICROBIAL ACTIVITY;

ANTIBIOTIC BIOSYNTHESIS; ARTICLE; BACTERIAL STRAIN; BIOSYNTHESIS; CONTROLLED STUDY; DNA TEMPLATE; ENZYME ACTIVITY; GENE DELETION; GENE OVEREXPRESSION; GENETIC TRANSCRIPTION; NONHUMAN; PLASMID; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; STREPTOMYCES AVERMITILIS;

BACTERIA (MICROORGANISMS); STREPTOMYCES AVERMITILIS;

EID: 84905972770     PISSN: 01757598     EISSN: 14320614     Source Type: Journal    
DOI: 10.1007/s00253-014-5759-7     Document Type: Article

References (35)

1. Bentley SD, Chater KF, Cerdeno-Tarraga AM, Challis GL, Thomson NR, James KD, Harris DE, Quail MA, Kieser H, Harper D (2002) Complete genome sequence of the model actinomycete Streptomyces coelicolor A3(2). Nature 417:141-147 (Pubitemid 34506788)
2. Bierman M, Logan R, O'Brien K, Seno ET, Rao RN, Schoner BE (1992) Plasmid cloning vectors for the conjugal transfer of DNA from Escherichia coli to Streptomyces spp. Gene 116:43-49
3. Burg RW, Miller BM, Baker EE, Birnbaum J, Currie SA, Hartman R, Kong YL, Monaghan RL, Olson G, Putter I, Tunac JB, Wallick H, Stapley EO, Oiwa R, Omura S (1979) Avermectins, new family of potent anthelmintic agents: producing organism and fermentation. Antimicrob Agents Chemother 15:361-367 (Pubitemid 9206227)
4. Cao M, Wang T, Ye R, Helmann JD (2002) Antibiotics that inhibit cell wall biosynthesis induce expression of the Bacillus subtilis sigma (W) and sigma (M) regulons. Mol Microbiol 45:1267-1276 (Pubitemid 35015351)
5. E-mediated envelope stress response in Escherichia coli. Proc Natl Acad Sci U S A 108:2106-2111
6. Chen Z, Wen J, Song Y, Wen Y, Li JL (2007) Enhancement and selective production of avermectin B by recombinants of Streptomyces avermitilis via intraspecific protoplast fusion. Chin Sci Bull 52:616-622 (Pubitemid 46364929)
7. Francez-Charlot A, Frunzke J, Reichen C, Ebneter JZ, Gourion B, Vorholt JA (2009) Sigma factor mimicry involved in regulation of general stress response. Proc Natl Acad Sci U S A 106:3467-3472
8. Guo J, Zhao JL, Li LL, Chen Z, Wen Y, Li JL (2010) The pathway-specific regulator AveR from Streptomyces avermitilis positively regulates avermectin production while it negatively affects oligomycin biosynthesis. Mol Genet Genomics 283:123-133
9. Guo J, Zhang X, Luo S, He F, Chen Z, Wen Y, Li JL (2013) A novel TetR family transcriptional regulator, SAV576, negatively controls avermectin biosynthesis in Streptomyces avermitilis. PLoS One 8:e71330
10. Hong HJ, Paget MS, Buttner MJ (2002) A signal transduction system in Streptomyces coelicolor that activates the expression of a putative cell wall glycan operon in response to vancomycin and other cell wall-specific antibiotics. Mol Microbiol 44:1199-1211 (Pubitemid 34595753)
11. Hutchings MI, Hong HJ, Leibovitz E, Sutcliffe IC, Buttner MJ (2006) The sigma (E) cell envelope stress response of Streptomyces coelicolor is influenced by a novel lipoprotein, CseA. J Bacteriol 188:7222-7229 (Pubitemid 44547627)
12. Ikeda H, Kotaki H, Tanaka H, Omura S (1988) Involvement of glucose catabolism in avermectin production by Streptomyces avermitilis. Antimicrob Agents Chemother 32:282-284 (Pubitemid 18061395)
13. Ikeda H, Ishikawa J, Hanamoto A, Shinose M, Kikuchi H, Shiba T, Sakaki Y, Hattori M, Omura S (2003) Complete genome sequence and comparative analysis of the industrial microorganism Streptomyces avermitilis. Nat Biotechnol 21:526-531 (Pubitemid 36532017)
14. Jiang LB, Liu YP, Wang P, Wen Y, Song Y, Chen Z, Li JL (2011) Inactivation of the extracytoplasmic function sigma factor Sig6 stimulates avermectin production in Streptomyces avermitilis. Biotechnol Lett 33:1955-1961
15. Kieser T, Bibb MJ, Buttner MJ, Chater KF, Hopwood DA (2000) Practical Streptomyces genetics: a laboratory manual. John Innes Foundation, Norwich
16. Kitani S, Ikeda H, Sakamoto T, Noguchi S, Nihira T (2009) Characterization of a regulatory gene, aveR, for the biosynthesis of avermectin in Streptomyces avermitilis. Appl Microbiol Biotechnol 82:1089-1096
17. Li W, Stevenson CE, Burton N, Jakimowicz P, Paget MS, Buttner MJ, Lawson DM, Kleanthous C (2002) Identification and structure of the anti-sigma factor-binding domain of the disulphide-stress regulated sigma factor σR from Streptomyces coelicolor. JMol Biol 323:225-236 (Pubitemid 35283688)
18. Li LL, Guo J, Wen Y, Chen Z, Song Y, Li JL (2010) Overexpression of ribosome recycling factor causes increased production of avermectin in Streptomyces avermitilis strains. J Ind Microbiol Biotechnol 37:673-679
19. Lin XP, Wen Y, Li M, Chen Z, Guo J, Song Y, Li JL (2009) A new strain of Streptomyces avermitilis produces high yield of oligomycin A with potent anti-tumor activity on human cancer cell lines in vitro. Appl Microbiol Biotechnol 81:839-845
20. Macneil DJ, Klapko LM (1987) Transformation of Streptomyces avermitilis by plasmid DNA. J Ind Microbiol 2:209-218
21. Mascher T (2013) Signaling diversity and evolution of extracytoplasmic function (ECF) σ factors. Curr Opin Microbiol 16:148-155
22. Meng XD, Michael HB, Scot AW (2005) A bacterial one-hybrid system for determining the DNA-binding specificity of transcription factors. Nat Biotechnol 23:988-994
23. Omura S, Ikeda H, Ishikawa J, Hanamoto A, Takahashi C, Shinose M, Takahashi Y, Horikawa H, Nakazawa H, Osonoe T, Kikuchi H, Shiba T, Sakaki Y, Hattori M (2001) Genome sequence of an industrial microorganism Streptomyces avermitilis: deducing the ability of producing secondary metabolites. Proc Natl Acad Sci U S A 98:12215-12220 (Pubitemid 32959853)
24. E is required for normal cell wall structure in Streptomyces coelicolor A3(2). J Bacteriol 181:204-211
25. Pinna LA, Lorini M, Moret V, Siliprandi N (1967) Effect of oligomycin and succinate on mitochondrial metabolism of adenine nucleotides. Biochim Biophys Acta 143:18-25
26. Sambrook J, MacCallum P, and Russell D (2001) Molecular cloning: a laboratory manual, third ed. Cold Spring Harbor Laboratory Press
27. Shu D, Chen L, Wang W, Yu Z, Ren C, Zhang W, Yang S, Lu Y, Jiang W (2009) 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 81:1149-1160
28. Staron A, Sofia HJ, Dietrich S, Ulrich LE, Liesegang H, 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
29. Tiffert Y, Supra P, Wurm R, Wohlleben W, Wagner R, Reuther J (2008) The Streptomyces coelicolor GlnR regulon: identification of new GlnR targets and evidence for a central role of GlnR in nitrogen metabolism in actinomycetes. Mol Microbiol 67:861-880 (Pubitemid 351143689)
30. Wang R, Mast Y, Wang J, Zhang W, Zhao G, Wohlleben W, Lu Y, Jiang W (2013) Identification of two-component system AfsQ1/Q2 regulon and its cross-regulation with GlnR in Streptomyces coelicolor. Mol Microbiol 87:30-48
31. Yu Q, Bai LQ, Zhou XF, Deng ZX (2012) Inactivation of the positive LuxR-type oligomycin biosynthesis regulators OlmRI and OlmRII increases avermectin production in Streptomyces avermitilis. Chin Sci Bull 8:869-876
32. Zhao JL, Wen Y, Chen Z, Song Y, Li JL (2007) An adpA homologue in Streptomyces avermitilis is involved in regulation of morphogenesis and melanogenesis. Chin Sci Bull 52:623-630 (Pubitemid 46364930)
33. Zhuo Y, Zhang W, Chen D, Gao H, Tao J, Liu M, Gou Z, Zhou X, Ye BC, Zhang Q, Zhang S, Zhang LX (2010) Reverse biological engineering of hrdB to enhance the production of avermectins in an industrial strain of Streptomyces avermitilis. Proc Natl Acad Sci U S A 107:11250-11254
34. Zianni M, Tessanne K, Merighi M, Laguna R, Tabita FR (2006) Identification of the DNA bases of a DNase I footprint by the use of dye primer sequencing on an automated capillary DNA analysis instrument. J Biomol Tech 17:103-113
35. Zweers JC, Nicolas P, Wiegert T, van Dijl JM, Denham EL (2012) Definition of the σ (W) regulon of Bacillus subtilis in the absence of stress. PLoS One 7:e48471