Secondary Metabolites Produced during the Germination of Streptomyces coelicolor

. 2017 ; 8 () : 2495. [epub] 20171213

Status PubMed-not-MEDLINE Jazyk angličtina Země Švýcarsko Médium electronic-ecollection

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid29326665

Spore awakening is a series of actions that starts with purely physical processes and continues via the launching of gene expression and metabolic activities, eventually achieving a vegetative phase of growth. In spore-forming microorganisms, the germination process is controlled by intra- and inter-species communication. However, in the Streptomyces clade, which is capable of developing a plethora of valuable compounds, the chemical signals produced during germination have not been systematically studied before. Our previously published data revealed that several secondary metabolite biosynthetic genes are expressed during germination. Therefore, we focus here on the secondary metabolite production during this developmental stage. Using high-performance liquid chromatography-mass spectrometry, we found that the sesquiterpenoid antibiotic albaflavenone, the polyketide germicidin A, and chalcone are produced during germination of the model streptomycete, S. coelicolor. Interestingly, the last two compounds revealed an inhibitory effect on the germination process. The secondary metabolites originating from the early stage of microbial growth may coordinate the development of the producer (quorum sensing) and/or play a role in competitive microflora repression (quorum quenching) in their nature environments.

Zobrazit více v PubMed

Alvarez-Alvarez R., Botas A., Albillos S. M., Rumbero A., Martin J. F., Liras P. (2015). Molecular genetics of naringenin biosynthesis, a typical plant secondary metabolite produced by Streptomyces clavuligerus. Microb. Cell Fact. 14:178. 10.1186/s12934-015-0373-7 PubMed DOI PMC

Aoki Y., Matsumoto D., Kawaide H., Natsume M. (2011). Physiological role of germicidins in spore germination and hyphal elongation in Streptomyces coelicolor A3(2). J. Antibiot. 64, 607–611. 10.1038/ja.2011.59 PubMed DOI

Aoki Y., Yoshida M., Kawaide H., Abe H., Natsume M. (2007). Isolation and characterization of a spore germination inhibitor from Streptomyces sp. CB-1-1, a phytopathogen causing root tumor of melon. Biosci. Biotechnol. Biochem. 71, 986–992. 10.1271/bbb.60649 PubMed DOI

Avé D. A., Gregory P., Tingey W. M. (1987). Aphid repellent sesquiterpenes in glandular trichomes of Solanum berthaultii and S. tuberosum. Entomol. Experim. Appl. 44, 131–138. 10.1111/j.1570-7458.1987.tb01057.x DOI

Baltz R. H. (2008). Renaissance in antibacterial discovery from actinomycetes. Curr. Opin. Pharmacol. 8, 557–563. 10.1016/j.coph.2008.04.008 PubMed DOI

Bentley S. D., Chater K. F., Cerdeno-Tarraga A. M., Challis G. L., Thomson N. R., James K. D., et al. . (2002). Complete genome sequence of the model actinomycete Streptomyces coelicolor A3(2). Nature 417, 141–147. 10.1038/417141a PubMed DOI

Bobek J., Halada P., Angelis J., Vohradsky J., Mikulik K. (2004). Activation and expression of proteins during synchronous germination of aerial spores of Streptomyces granaticolor. Proteomics 4, 3864–3880. 10.1002/pmic.200400818 PubMed DOI

Bobek J., Šmídová K., Čihák M. (2017). A waking review: old and novel insights into the spore germination in Streptomyces. Front. Microbiol. 8:2205. 10.3389/fmicb.2017.02205 PubMed DOI PMC

Bobek J., Strakova E., Zikova A., Vohradsky J. (2014). Changes in activity of metabolic and regulatory pathways during germination of S. coelicolor. BMC Genomics 15:1173. 10.1186/1471-2164-15-1173 PubMed DOI PMC

Brachmann A. O., Brameyer S., Kresovic D., Hitkova I., Kopp Y., Manske C., et al. . (2013). Pyrones as bacterial signaling molecules. Nat. Chem. Biol. 9, 573–578. 10.1038/nchembio.1295 PubMed DOI

Burdock T. J., Brooks M. S., Ghaly A. E. (2011). A dehydrogenase activity test for monitoring the growth of Streptomyces venezuelae in a nutrient rich medium. J. Bioprocess Biotechniq. 1:101 10.4172/2155-9821.1000101 DOI

Bystrykh L. V., Fernandez-Moreno M. A., Herrema J. K., Malpartida F., Hopwood D. A., Dijkhuizen L. (1996). Production of actinorhodin-related "blue pigments" by Streptomyces coelicolor A3(2). J. Bacteriol. 178, 2238–2244. 10.1128/jb.178.8.2238-2244.1996 PubMed DOI PMC

Camilli A., Bassler B. L. (2006). Bacterial small-molecule signaling pathways. Science 311, 1113–1116. 10.1126/science.1121357 PubMed DOI PMC

Chemler J. A., Buchholz T. J., Geders T. W., Akey D. L., Rath C. M., Chlipala G. E., et al. . (2012). Biochemical and structural characterization of germicidin synthase: analysis of a type III polyketide synthase that employs acyl-ACP as a starter unit donor. J. Am. Chem. Soc. 134, 7359–7366. 10.1021/ja2112228 PubMed DOI PMC

Chen K. C., Csikasz-Nagy A., Gyorffy B., Val J., Novak B., Tyson J. J. (2000). Kinetic analysis of a molecular model of the budding yeast cell cycle. Mol. Biol. Cell 11, 369–391. 10.1091/mbc.11.1.369 PubMed DOI PMC

Claessen D., de Jong W., Dijkhuizen L., Wosten H. A. (2006). Regulation of Streptomyces development: reach for the sky! Trends Microbiol. 14, 313–319. 10.1016/j.tim.2006.05.008 PubMed DOI

Davis N. K., Chater K. F. (1990). Spore colour in Streptomyces coelicolor A3(2) involves the developmentally regulated synthesis of a compound biosynthetically related to polyketide antibiotics. Mol. Microbiol. 4, 1679–1691. 10.1111/j.1365-2958.1990.tb00545.x PubMed DOI

Derouaux A., Halici S., Nothaft H., Neutelings T., Moutzourelis G., Dusart J., et al. . (2004). Deletion of a cyclic AMP receptor protein homologue diminishes germination and affects morphological development of Streptomyces coelicolor. J. Bacteriol. 186, 1893–1897. 10.1128/JB.186.6.1893-1897.2004 PubMed DOI PMC

Diaz-Tielas C., Grana E., Reigosa M. J., Sanchez-Moreiras A. M. (2012). The role of peroxidases on the mode of action of chalcone in Arabidopsis roots. Plant Signal. Behav. 7, 1274–1276. 10.4161/psb.21594 PubMed DOI PMC

Eaton D., Ensign J. C. (1980). Streptomyces viridochromogenes spore germination initiated by calcium ions. J. Bacteriol. 143, 377–382. PubMed PMC

Funa N., Ohnishi Y., Fujii I., Shibuya M., Ebizuka Y., Horinouchi S. (1999). A new pathway for polyketide synthesis in microorganisms. Nature 400, 897–899. 10.1038/23748 PubMed DOI

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. 10.1128/mBio.00407-12 PubMed DOI PMC

Gerber N. N., Lechevalier H. A. (1965). Geosmin, an earthly-smelling substance isolated from actinomycetes. Appl. Microbiol. 13, 935–938. PubMed PMC

Gibson R. W., Pickett J. A. (1983). Wild potato repels aphids by release of aphid alarm pheromone. Nature 302, 608–609. 10.1038/302608a0 DOI

Gomez-Escribano J. P., Song L., Fox D. J., Yeo V., Bibb M. J., Challis G. (2012). Structure and biosynthesis of the unusual polyketide alkaloid coelimycin P1, a metabolic product of the cpk gene cluster of Streptomyces coelicolor M145. Chem. Sci. 3, 2716–2720. 10.1039/c2sc20410j DOI

Grund A. D., Ensign J. C. (1985). Properties of the germination inhibitor of Streptomyces viridochromogenes spores. J. Gen. Microbiol. 131, 833–847. 10.1099/00221287-131-4-833 PubMed DOI

Gurtler H., Pedersen R., Anthoni U., Christophersen C., Nielsen P. H., Wellington E. M., et al. . (1994). Albaflavenone, a sesquiterpene ketone with a zizaene skeleton produced by a streptomycete with a new rope morphology. J. Antibiot. 47, 434–439. 10.7164/antibiotics.47.434 PubMed DOI

Haiser H. J., Yousef M. R., Elliot M. A. (2009). Cell wall hydrolases affect germination, vegetative growth, and sporulation in Streptomyces coelicolor. J. Bacteriol. 191, 6501–6512. 10.1128/JB.00767-09 PubMed DOI PMC

Hirsch C. F., Ensign J. C. (1976a). Heat activation of Streptomyces viridochromogenes spores. J. Bacteriol. 126, 24–30. PubMed PMC

Hirsch C. F., Ensign J. C. (1976b). Nutritionally defined conditions for germination of Streptomyces viridochromogenes spores. J. Bacteriol. 126, 13–23. PubMed PMC

Hirsch C. F., Ensign J. C. (1978). Some properties of Streptomyces viridochromogenes spores. J. Bacteriol. 134, 1056–1063. PubMed PMC

Hodgson D. (1982). Glucose repression of carbon source uptake and metabolism in Streptomyces coelicolor A3(2) and its perturbation in mutants resistant to 2-deoxyglucose. Micro Soc. 128, 2417–2430. 10.1099/00221287-128-10-2417 DOI

Hopwood D. A. (2007). How do antibiotic-producing bacteria ensure their self-resistance before antibiotic biosynthesis incapacitates them? Mol. Microbiol. 63, 937–940. 10.1111/j.1365-2958.2006.05584.x PubMed DOI

Ikeda H., Ishikawa J., Hanamoto A., Shinose M., Kikuchi H., Shiba T., et al. . (2003). Complete genome sequence and comparative analysis of the industrial microorganism Streptomyces avermitilis. Nat. Biotechnol. 21, 526–531. 10.1038/nbt820 PubMed DOI

Izumikawa M., Shipley P. R., Hopke J. N., O'Hare T., Xiang L., Noel J. P., et al. . (2003). Expression and characterization of the type III polyketide synthase 1,3,6,8-tetrahydroxynaphthalene synthase from Streptomyces coelicolor A3(2). J. Ind. Microbiol. Biotechnol. 30, 510–515. 10.1007/s10295-003-0075-8 PubMed DOI

Janecek J., Tichy P., Spizek J., Vanek Z. (1997). Constitution of the metabolic type of streptomycetes during the first hours of cultivation. Folia Microbiol. 42, 75–96. 10.1007/BF02898713 PubMed DOI

Kalan L., Gessner A., Thaker M. N., Waglechner N., Zhu X., Szawiola A., et al. . (2013). A cryptic polyene biosynthetic gene cluster in Streptomyces calvus is expressed upon complementation with a functional bldA gene. Chem. Biol. 20, 1214–1224. 10.1016/j.chembiol.2013.09.006 PubMed DOI

Kamenik Z., Hadacek F., Mareckova M., Ulanova D., Kopecky J., Chobot V., et al. . (2010). Ultra-high-performance liquid chromatography fingerprinting method for chemical screening of metabolites in cultivation broth. J. Chromatogr. A 1217, 8016–8025. 10.1016/j.chroma.2010.08.031 PubMed DOI

Kelemen G. H., Buttner M. J. (1998). Initiation of aerial mycelium formation in Streptomyces. Curr. Opin. Microbiol. 1, 656–662. 10.1016/S1369-5274(98)80111-2 PubMed DOI

Keller N. P., Turner G., Bennett J. W. (2005). Fungal secondary metabolism - from biochemistry to genomics. Nat. Rev. Microbiol. 3, 937–947. 10.1038/nrmicro1286 PubMed DOI

Kieser T., Bibb M. J., Buttner M. J., Chater K. F., Hopwood D. A. (2000). Practical Streptomyces Genetics, 2nd Edn. Norwich: John Innes Foundation.

Lakey J. H., Lea E. J., Rudd B. A., Wright H. M., Hopwood D. A. (1983). A new channel-forming antibiotic from Streptomyces coelicolor A3(2) which requires calcium for its activity. J. Gen. Microbiol. 129, 3565–3573. 10.1099/00221287-129-12-3565 PubMed DOI

Lee K. J., Rho Y. T. (1993). Characteristics of spores formed by surface and submerged cultures of Streptomyces albidoflavus SMF301. J. Gen. Microbiol. 139, 3131–3137. 10.1099/00221287-139-12-3131 DOI

Luo Y., Huang H., Liang J., Wang M., Lu L., Shao Z., et al. . (2013). Activation and characterization of a cryptic polycyclic tetramate macrolactam biosynthetic gene cluster. Nat. Commun. 4:894. 10.1038/ncomms3894 PubMed DOI PMC

Ma M., Rateb M. E., Yang D., Rudolf J. D., Zhu X., Huang Y., et al. . (2017). Germicidins H-J from Streptomyces sp. CB00361. J. Antibiot. 70, 200–203. 10.1038/ja.2016.100 PubMed DOI

Martinez G., Regente M., Jacobi S., Del Rio M., Pinedo M., de la Canal L. (2017). Chlorogenic acid is a fungicide active against phytopathogenic fungi. Pestic. Biochem. Physiol. 140, 30–35. 10.1016/j.pestbp.2017.05.012 PubMed DOI

Maxwell C. A., Hartwig U. A., Joseph C. M., Phillips D. A. (1989). A chalcone and two related flavonoids released from alfalfa roots induce nod genes of rhizobium meliloti. Plant Physiol. 91, 842–847. 10.1104/pp.91.3.842 PubMed DOI PMC

McCormick J. R., Flardh K. (2012). Signals and regulators that govern Streptomyces development. FEMS Microbiol. Rev. 36, 206–231. 10.1111/j.1574-6976.2011.00317.x PubMed DOI PMC

Mikulik K., Bobek J., Bezouskova S., Benada O., Kofronova O. (2002). Expression of proteins and protein kinase activity during germination of aerial spores of Streptomyces granaticolor. Biochem. Biophys. Res. Commun. 299, 335–342. 10.1016/S0006-291X(02)02606-2 PubMed DOI

Mikulik K., Bobek J., Zikova A., Smetakova M., Bezouskova S. (2011). Phosphorylation of ribosomal proteins influences subunit association and translation of poly (U) in Streptomyces coelicolor. Mol. Biosyst. 7, 817–823. 10.1039/C0MB00174K PubMed DOI

Mikulik K., Janda I., Maskova H., Stastna J., Jiranova A. (1977). Macromolecular synthesis accompanying the transition from spores to vegetative forms of Streptomyces granaticolor. Folia Microbiol. 22, 252–261. 10.1007/BF02877654 PubMed DOI

Mikulik K., Paleckova P., Felsberg J., Bobek J., Zidkova J., Halada P. (2008). SsrA genes of streptomycetes and association of proteins to the tmRNA during development and cellular differentiation. Proteomics 8, 1429–1441. 10.1002/pmic.200700560 PubMed DOI

Moody S. C., Zhao B., Lei L., Nelson D. R., Mullins J. G., Waterman M. R., et al. . (2012). Investigating conservation of the albaflavenone biosynthetic pathway and CYP170 bifunctionality in streptomycetes. FEBS J. 279, 1640–1649. 10.1111/j.1742-4658.2011.08447.x PubMed DOI

Ohnishi Y., Ishikawa J., Hara H., Suzuki H., Ikenoya M., Ikeda H., et al. . (2008). Genome sequence of the streptomycin-producing microorganism Streptomyces griseus IFO 13350. J. Bacteriol. 190, 4050–4060. 10.1128/JB.00204-08 PubMed DOI PMC

Okamoto S., Taguchi T., Ochi K., Ichinose K. (2009). Biosynthesis of actinorhodin and related antibiotics: discovery of alternative routes for quinone formation encoded in the act gene cluster. Chem. Biol. 16, 226–236. 10.1016/j.chembiol.2009.01.015 PubMed DOI

Paleckova P., Bobek J., Felsberg J., Mikulik K. (2006). Activity of translation system and abundance of tmRNA during development of Streptomyces aureofaciens producing tetracycline. Folia Microbiol. 51, 517–524. 10.1007/BF02931615 PubMed DOI

Petersen F., Zahner H., Metzger J. W., Freund S., Hummel R. P. (1993). Germicidin, an autoregulative germination inhibitor of Streptomyces viridochromogenes NRRL B-1551. J. Antibiot. 46, 1126–1138. 10.7164/antibiotics.46.1126 PubMed DOI

Phelan V. V., Liu W. T., Pogliano K., Dorrestein P. C. (2011). Microbial metabolic exchange–the chemotype-to-phenotype link. Nat. Chem. Biol. 8, 26–35. 10.1038/nchembio.739 PubMed DOI PMC

Rajan B. M., Kannabiran K. (2014). Extraction and identification of antibacterial secondary metabolites from marine Streptomyces sp. VITBRK2. Int. J. Mol. Cell. Med. 3, 130–137. PubMed PMC

Ranade N., Vining L. C. (1993). Accumulation of intracellular carbon reserves in relation to chloramphenicol biosynthesis by Streptomyces venezuelae. Can. J. Microbiol. 39, 377–383. 10.1139/m93-055 PubMed DOI

Romero-Rodriguez A., Ruiz-Villafan B., Tierrafria V. H., Rodriguez-Sanoja R., Sanchez S. (2016). Carbon catabolite regulation of secondary metabolite formation and morphological differentiation in Streptomyces coelicolor. Appl. Biochem. Biotechnol. 180, 1152–1166. 10.1007/s12010-016-2158-9 PubMed DOI

Rutherford S. T., Bassler B. L. (2012). Bacterial quorum sensing: its role in virulence and possibilities for its control. Cold Spring Harb. Perspect. Med. 2:a012427. 10.1101/cshperspect.a012427 PubMed DOI PMC

Schaberle T. F. (2016). Biosynthesis of alpha-pyrones. Beilstein J. Org. Chem. 12, 571–588. 10.3762/bjoc.12.56 PubMed DOI PMC

Schenck F. J., Hobbs J. E. (2004). Evaluation of the quick, easy, cheap, effective, rugged, and safe (QuEChERS) approach to pesticide residue analysis. Bull. Environ. Contam. Toxicol. 73, 24–30. 10.1007/s00128-004-0388-y PubMed DOI

Seipke R. F., Kaltenpoth M., Hutchings M. I. (2012). Streptomyces as symbionts: an emerging and widespread theme? FEMS Microbiol. Rev. 36, 862–876. 10.1111/j.1574-6976.2011.00313.x PubMed DOI

Sello J. K., Buttner M. J. (2008). The gene encoding RNase III in Streptomyces coelicolor is transcribed during exponential phase and is required for antibiotic production and for proper sporulation. J. Bacteriol. 190, 4079–4083. 10.1128/JB.01889-07 PubMed DOI PMC

Shima J., Hesketh A., Okamoto S., Kawamoto S., Ochi K. (1996). Induction of actinorhodin production by rpsL (encoding ribosomal protein S12) mutations that confer streptomycin resistance in Streptomyces lividans and Streptomyces coelicolor A3(2). J. Bacteriol. 178, 7276–7284. 10.1128/jb.178.24.7276-7284.1996 PubMed DOI PMC

Sivakumar P. M., Priya S., Doble M. (2009). Synthesis, biological evaluation, mechanism of action and quantitative structure-activity relationship studies of chalcones as antibacterial agents. Chem. Biol. Drug Des. 73, 403–415. 10.1111/j.1747-0285.2009.00793.x PubMed DOI

Strakova E., Bobek J., Zikova A., Rehulka P., Benada O., Rehulkova H., et al. . (2013). Systems insight into the spore germination of Streptomyces coelicolor. J. Proteome Res. 12, 525–536. 10.1021/pr300980v PubMed DOI

Strakova E., Zikova A., Vohradsky J. (2014). Inference of sigma factor controlled networks by using numerical modeling applied to microarray time series data of the germinating prokaryote. Nucleic Acids Res. 42, 748–763. 10.1093/nar/gkt917 PubMed DOI PMC

Tahlan K., Ahn S. K., Sing A., Bodnaruk T. D., Willems A. R., Davidson A. R., et al. . (2007). Initiation of actinorhodin export in Streptomyces coelicolor. Mol. Microbiol. 63, 951–961. 10.1111/j.1365-2958.2006.05559.x PubMed DOI

Tanaka Y., Kasahara K., Hirose Y., Murakami K., Kugimiya R., Ochi K. (2013). Activation and products of the cryptic secondary metabolite biosynthetic gene clusters by rifampin resistance (rpoB) mutations in actinomycetes. J. Bacteriol. 195, 2959–2970. 10.1128/JB.00147-13 PubMed DOI PMC

van Keulen G., Dyson P. J. (2014). Production of specialized metabolites by Streptomyces coelicolor A3(2). Adv. Appl. Microbiol. 89, 217–266. 10.1016/B978-0-12-800259-9.00006-8 PubMed DOI

van Vliet S. (2015). Bacterial dormancy: how to decide when to wake up. Curr. Biol. 25, R753–R755. 10.1016/j.cub.2015.07.039 PubMed DOI

Wakefield J., Hassan H. M., Jaspars M., Ebel R., Rateb M. E. (2017). Dual induction of new microbial secondary metabolites by fungal bacterial co-cultivation. Front. Microbiol. 8:1284. 10.3389/fmicb.2017.01284 PubMed DOI PMC

Waters C. M., Bassler B. L. (2005). Quorum sensing: cell-to-cell communication in bacteria. Annu. Rev. Cell Dev. Biol. 21, 319–346. 10.1146/annurev.cellbio.21.012704.131001 PubMed DOI

Xu Y., Vetsigian K. (2017). Phenotypic variability and community interactions of germinating Streptomyces spores. Sci. Rep. 7:699. 10.1038/s41598-017-00792-7 PubMed DOI PMC

Ylstra B., Touraev A., Moreno R. M., Stoger E., van Tunen A. J., Vicente O., et al. . (1992). Flavonols stimulate development, germination, and tube growth of tobacco pollen. Plant Physiol. 100, 902–907. 10.1104/pp.100.2.902 PubMed DOI PMC

Yoshida M., Kobayashi K. (1994). Morphogenesis of the pathogenic Streptomyces sp. causing root tumor of melon on the ulture medium. Ann. Phytopathol. Soc. Jpn. 60, 514–522. 10.3186/jjphytopath.60.514 DOI

Zhao B., Lei L., Vassylyev D. G., Lin X., Cane D. E., Kelly S. L., et al. . (2009). Crystal structure of albaflavenone monooxygenase containing a moonlighting terpene synthase active site. J. Biol. Chem. 284, 36711–36719. 10.1074/jbc.M109.064683 PubMed DOI PMC

Najít záznam

Citační ukazatele

Nahrávání dat ...

Možnosti archivace

Nahrávání dat ...