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Goadsporin, a Chemical Substance Which Promotes Secondary Metabolism and Morphogenesisin Streptomycetes

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Goadsporin, a Chemical Substance Which Promotes Secondary Metabolism and Morphogenesisin Streptomycetes VOL. 54 NO. 12, DEC. 2001 THE JOURNAL OF ANTIBIOTICS pp. 1036 - 1044 Goadsporin, a Chemical Substance which Promotes Secondary Metabolism and Morphogenesisin Streptomycetes I. Purification and Characterization Hiroyasu Onaka* , Hirokazu Tabata, Yasuhiro Igarashi, Yukio SAroa and Tamotsu Furumai Biotechnology Research Center, ToyamaPrefectural University, a College of Technology, ToyamaPrefectural University, 5 1 80 Kurokawa, Kosugi, Toyama 939-0398, Japan (Received for publication July 30, 2001) Streptomycetes, which belong to the Gram-positive bacteria, produce secondary metabolites and sporulate. The timing of starting the secondary metabolite production and the sporulation depends on environmental conditions such as nitrogen and carbon sources. In order to obtain a tool for understanding the regulation mechanism, we carried out screening for chemical substances that induce secondary metabolism and sporulation in streptomycetes and found an active substance from the culture broth of Streptomyces sp. TP-A0584. This substance designated goadsporin promoted the formation of red pigment and sporulation at a concentration of 1 jim in Streptomyces lividans TK23 which does not produce the pigment under normal growth conditions. Goadsporin is an oligopeptide consisting of 19 amino acids with the molecular formula C72H97N19O20S2. Sporulation and/or secondary metabolite production was induced in 36 streptomycetes strains among 42 strains tested. These results suggest that goadsporin acts on a commonregulation pathwayfor sporulation and secondary metabolism in streptomycetes and can be a powerful tool to analyze the regulation mechanism. A number of antibiotics and other bioactive molecules metabolism and cell differentiation in streptomycetes1'2^ with a variety of chemical structures have been found from For example, in Streptomyces griseus, Streptomyces actinomycetes as their secondary metabolites. Owingto this virginiae and Streptomyces coelicolor A3(2), low diversity, extensive screening for bioactive compounds molecular-weight substances containing a butyrolactone from actinomycetes has been conducted, aiming at serve as chemical signal molecules or microbial hormones pharmaceutical usage. In screening of soil-derived for secondary metabolism and/or cellular differentiation3'4^ actinomycetes, it is widely recognized that growth In addition, eukaryotic protein kinases5) and sigma conditions influence the production of secondary cascades6) are shownto exist as commoncomponentsin the metabolites because actinomycetes regulate secondary regulatory pathway. metabolism and morphogenesis in response to S. lividans is known to possess a complete set of the environmental conditions. In industrial fermentation, biosynthetic genes for actinorhodin, a red pigment, physical and chemical conditions such as temperature, although it dose not produce the pigment under aeration and medium composition are strictly controlled to conventional growth conditions. Interestingly, it is reported gain the maximumproductivity. that the afsR gene that was cloned from S. coelicolor A3(2) In recent years, molecular microbiological studies have stimulates actinorhodin production in S. lividans1^. This disclosed commonregulation systems for secondary result shows that S. lividans has the potential to produce * Corresponding author: [email protected] VOL.54 NO. 12 THE JOURNAL OF ANTIBIOTICS 1037 actinorhodin under specific conditions while the production consisted of Yeast extract (Difco) 0.1%, Meat extract is repressed under usual conditions. (Wako Pure Chemicals) 0.1%, NZ amine 0.2%, glucose There are several reports on small molecules that induce 1.0% (pH 7.2). Nutrient Broth agar was purchased from the secondary metabolism and/or cell differentiation in Difco Lab. streptomycetes. A-factor, the most well known Bacterial strains used in this study are shown in Table 1. butyrolactone, induces streptomycin production, ATCC strains were obtained from the American Type streptomycin resistance, yellow pigment production and Culture Collection, Rockville, MD.IFO strains were aerial myceliumformation at a concentration of less than obtained from the Institution of Fermentation, Osaka, 1 nMin S. griseus*~l0\ Virginia butanolide and IM-2, other Japan. A NRRLstrain was obtained from the Northern butyrolactones, induce the production of virginiamycin in Utilization Research and Development Division, U.S. S. virginiae, and those of showdomycin and minimycin in Department of Agriculture, Peoria, IL. S. lavendulae, respectively11>12). Recently, homologues of the A-factor receptor gene were cloned from S. coelicolor Sample Preparation for Paper Disc Diffusion Assay A3(2) and shown to be involved in pigment production and Actinomycete strains isolated from soil samples cell differentiation13). These findings suggest that small collected in Kosugi-machi, Toyama prefecture, Japan, were molecules containing a butyrolactone moiety are widely used for screening. The isolated strains were inoculated into distributed in streptomycetes as microbial hormones. Their 500-ml K-l flasks containing 100ml of V-22 medium. hormone-like activity is observed only against the After incubation at 30°C for 4 days on a rotary shaker at hormone-producing strain itself but not against the non- 200 rpm, 5-ml aliquots of this seed culture were transferred producing streptomycetes, indicating a high specificity in into 500-ml K-l flasks, each containing 100ml of A-3M the recognition of the butyrolactones. Pamamycin-607, medium. The fermentation was carried out at 30°C for 7 another signal molecule in streptomycetes, possesses a days on the same rotary shaker. The culture broth was sixteen-membered macrodiolide structure and was isolated extracted with 100ml of?z-butanol, and the extract was from Streptomyces alboniger IFO 1273814). This molecule subjected to the screening assay. induces aerial mycelium formation at 0.1 ^g/paper disc in its producing strain, but the activity is observed only with Assay Procedure for Secondary Metabolism and the producing strain. Sporulation Promoter To date there is no-.report on substances that induce Nutrient broth soft agar containing 10 spores of S. secondary metabolism and morphogenesis in a wide range lividans TK23 was overlaid on Bennett's agar plates, n- of Streptomyces species although the presence of a common Butanol extracts described above were absorbed in paper regulatory system is suggested in streptomycetes. In this discs (diameter: 10mm), and the discs dried, placed on the paper, our successful screening for such inducer from plates and incubated at 30°C. Pigment production and cell soil-derived actinomycetes, and the purification, differentiation around the paper disc wereobserved every characterization and biological activity of the novel inducer, 24 hours. Spore suspension was prepared according to the goadsporin, are described. procedure reported by D. A. Hopwoodet al.l5\ i Purification of Goadsporin / Materials and Methods The paper disc diffusion assay described above was used to detect the active fractions. The amountand purity of Media and Strains goadsporin was estimated by HPLCanalysis as described The production culture for actinomycetes was A-3M below. medium, consisting of glucose 0.5%, glycerol 2.0%, (i) Fermentation: Streptomyces sp. TP-A0584 was soluble starch 2.0%, pharmamedia 1.5%, Yeast extract inoculated into 500-ml K-l flasks containing 100ml of V- (Difco Laboratory, MI) 0.3% and Diaion HP-20 1.0% (pH 22 medium. After incubation at 30°C for 2 days on a rotary 7.0). The seed culture for actinomycetes was V-22 medium, shaker at 200rpm, 5-ml aliquots of the seed culture were consisting of soluble starch 1.0%, glucose 0.5%, NZ-case transferred into one hundred 500-ml K-l flasks, each 0.3%, Yeast extract (Difco) 0.2%, Bacto Tryptone 0.5%, containing 100 ml ofA-3M medium. The fermentation was K2HPO4 0.1%, MgSO4-7H2O 0.05% and CaCO3 0.3% (pH carried out at 30°C for 4 days. 7.0). Bennett's agar and Nutrient Broth agar medium were (ii) Diaion HP-20 column chromatography: The used for the paper disc diffusion assay. Bennett's agar cultured broth (10 liters) was centrifuged at; 5000X# for 10 1038 THE JOURNAL OF ANTIBIOTICS DEC. 2001 Table 1. Bacterial strains. Designation Relevant characteristics Source of reference Streptomyces sp. TP-A0584 goadsporin producer this study for goadsporin assay S. lividans TK23 goadsporin responder D. A. Hopwood S. spinicoumarensis ATCC2981 3 ATC C S. violaceoruber IFO15146 IFO S. griseolus NRRL3739 NRRL S. hygroscopicus TP-A0342 this study Microbispora sp. TP-A01 84 21 Streptomyces sp. TP-AO5 85 this study Streptomyces sp. TP-A05 86 this study Streptomyces sp. TP-A05 87 this study Streptomyces sp. TP-A0588 this study Streptomyces sp. TP-A05 89 this study Streptomyces sp. TP-A05 90 this study Streptomyces sp. TP-A059 1 this study strain TP-A0593 unidentified actinomycete this study for antibiotic and antifungal assay Streptomyces scabies JCM7914 Gram(+) JCM Bacillus subtilis ATCC6633 Gram(+) ATC C Escherichia coli NIHJ JCi2 Gram( -) Staphhylococcus aureus 209P JC- 1 Gram(-) Pseudomonas aeruginosa TP-B0270 Gram(- ) this study Proteus mirabilis ATCC21100 Gram(- ) ATCC Sacchromyces cerevisiae TP-F0 1 76 yeast cell this study Candida albicans TPi-F0594 yeast cell this study Cryptococcus neoformans ATCC901 1 2 yeast cell ATCC Torulopsis glabrata IFO0622 yeast cell IFO Aspergillus fumigatus IFO8866 filamentous fungi IFO minutes. The supernatant was discarded and the mycelial a gradient of chloroform-methanol
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