Genomic sequence-based discovery of novel angucyclinone antibiotics from marine Streptomyces sp. W007

FEMS Microbiology Letters

Volumn 332, Issue 2, 2012, Pages 105-112

  Zhang, Hongyu ^a,d   Wang, Hongbo ^c   Wang, Yipeng ^a   Cui, Hongli ^a   Xie, Zeping ^a   Pu, Yang ^a   Pei, Shiqian ^c   Li, Fuchao ^b   Qin, Song ^a  

^a YANTAI INSTITUTE OF COASTAL ZONE RESEARCH   (China)

^b INSTITUTE OF OCEANOLOGY   (China)

^c YANTAI UNIVERSITY   (China)

^d UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

Author keywords

Angucyclinone antibiotics; Antifungal activity; Cytotoxicity; Genome sequence; Polyketide

Indexed keywords

3 HYDROXY 1 KETO 3 METHYL 8 METHOXY 1,2,3,4 TETRAHYDRO BENZ[A]ANTHRACENE; ANGUCYCLINONE DERIVATIVE; ANTIBIOTIC AGENT; ANTINEOPLASTIC AGENT; ANTINEOPLASTIC ANTIBIOTIC; DOXORUBICIN; KIAMYCIN; POLYKETIDE SYNTHASE; UNCLASSIFIED DRUG;

ANTIFUNGAL ACTIVITY; ANTINEOPLASTIC ACTIVITY; BACTERIAL GENE; CONTROLLED STUDY; DRUG CYTOTOXICITY; DRUG DETERMINATION; DRUG DEVELOPMENT; DRUG EFFECT; DRUG MECHANISM; DRUG POTENCY; DRUG RESEARCH; DRUG SCREENING; DRUG STRUCTURE; GENE CLUSTER; GENE IDENTIFICATION; GENE SEQUENCE; GENOME ANALYSIS; HUMAN; HUMAN CELL; LETTER; NONHUMAN; NUCLEOTIDE SEQUENCE; POLYKETIDE SYNTHASE GENE; PRIORITY JOURNAL; SEQUENCE ANALYSIS; STREPTOMYCES; STRUCTURE ANALYSIS;

ANTHRAQUINONES; ANTIFUNGAL AGENTS; CHINA; DNA, BACTERIAL; GENES, BACTERIAL; GENOME, BACTERIAL; METABOLIC NETWORKS AND PATHWAYS; MULTIGENE FAMILY; SEAWATER; SEQUENCE ANALYSIS, DNA; STREPTOMYCES;

CLADOSPORIUM CUCUMERINUM; COLLETOTRICHUM LAGENARIUM; MONILINIA FRUCTICOLA; PHOMOPSIS ASPARAGI; POLYSTIGMA; STREPTOMYCES SP.;

EID: 84862607020     PISSN: 03781097     EISSN: 15746968     Source Type: Journal    
DOI: 10.1111/j.1574-6968.2012.02582.x     Document Type: Letter

References (48)

1. Ayuso A, Clark D, González I, Salazar O, Anderson A & Genilloud O (2005) A novel actinomycete strain de-replication approach based on the diversity of polyketide synthase and nonribosomal peptide synthetase biosynthetic pathways. Appl Microbiol Biotechnol 67: 795-806.
2. Banskota AH, McAlpine JB, Sørensen D et al. (2006) Isolation and identification of three new 5-alkenyl-3, 3 (2H)-furanones from two Streptomyces species using a genomic screening approach. J Antibiot 59: 168-176.
3. Bao Y, Zhang X, Zhao G & Ding X (2010) A S-adenosylmethionine dependent methyltransferase homologous gene, sco1162, regulates spore development and antibiotic synthesis in Streptomyces coelicolor. J Fudan Univ (Natural Science) 49: 552-557 (in Chinese with English abstract).
4. Basnet DB, Oh TJ, Vu TTH et al. (2006) Angucyclines Sch 47554 and Sch 47555 from Streptomyces sp. SCC-2136: cloning, sequencing, and characterization. Mol Cells 22: 154-162.
5. Bentley SD, Chater KF, Cerdeño-Tárraga AM et al. (2002) Complete genome sequence of the model actinomycete Streptomyces coelicolor A3 (2). Nature 417: 141-147.
6. Bérdy J (2005) Bioactive microbial metabolites. J Antibiot 58: 1-26.
7. Decker H & Haag S (1995) Cloning and characterization of a polyketide synthase gene from Streptomyces fradiae Tü2717, which carries the genes for biosynthesis of the angucycline antibiotic urdamycin A and a gene probably involved in its oxygenation. J Bacteriol 177: 6126-6136.
8. Delle Monache G, De Rosa MC, Scurria R, Monacelli B, Pasqua G, Dall'Olio G & Botta B (1991) Metabolites from in vitro cultures of Cassia didymobotrya. Phytochemistry 30: 1849-1854.
9. Dharmaraj S (2010) Marine Streptomyces as a novel source of bioactive substances. World J Microbiol Biotechnol 26: 2123-2139.
10. Fenical W & Jensen PR (2006) Developing a new resource for drug discovery: marine actinomycete bacteria. Nat Chem Biol 2: 666-673.
11. Fischbach MA & Walsh CT (2006) Assembly-line enzymology for polyketide and nonribosomal peptide antibiotics: logic, machinery, and mechanisms. Chem Rev 106: 3468-3496.
12. Galm U, Schimana J, Fiedler HP, Schmidt J, Li SM & Heide L (2002) Cloning and analysis of the simocyclinone biosynthetic gene cluster of Streptomyces antibioticus Tü 6040. Arch Microbiol 178: 102-114.
13. Gilpin ML, Balchin J, Box SJ & Tyler JW (1989) MM 47755, a new benz (a) anthracene antibiotic from a streptomycete. J Antibiot 42: 627-628.
14. Gould SJ, Hong ST & Carney JR (1998) Cloning and heterologous expression of genes from the kinamycin biosynthetic pathway of Streptomyces murayamaensis. J Antibiot 51: 50-57.
15. Han L, Yang K, Ramalingam E, Mosher RH & Vining LC (1994) Cloning and characterization of polyketide synthase genes for jadomycin B biosynthesis in Streptomyces venezuelae ISP5230. Microbiology 140: 3379-3389.
16. Ikeda H, Ishikawa J, Hanamoto A, Shinose M & Kikuchi H (2003) Complete genome sequence and comparative analysis of the industrial microorganism Streptomyces avermitilis. Nat Biotechnol 21: 526-531.
17. Kawasaki T, Hirashima R, Maruta T et al. (2010) Cloning and characterization of a gene cluster for hatomarubigin biosynthesis in Streptomyces sp. strain 2238-SVT4. Appl Environ Microbiol 76: 4201-4206.
18. Komaki H, Izumikawa M, Ueda JY, Nakashima T, Khan ST, Takagi M & Shin-ya K (2009) Discovery of a pimaricin analog JBIR-13, from Streptomyces bicolor NBRC 12746 as predicted by sequence analysis of type I polyketide synthase gene. Appl Microbiol Biotechnol 83: 127-133.
19. Li F, Maskey RP, Qin S et al. (2005) Chinikomycin A and B: isolation, structure elucidation and biological activity of novel antibiotics from a marine Streptomyces sp. isolate M045. J Nat Prod 68: 349-353.
20. Lin Y, Hao X, Johnstone L, Miller SJ, Baltrus DA, Rensing C & Wei G (2011) Draft genome of Streptomyces zinciresistens K42, a novel metal-resistant species isolated from copper-zinc mine tailings. J Bacteriol 193: 6408-6409.
21. Lombó F, Braña AF, Salas JA & Méndez C (2004) Genetic organization of the biosynthetic gene cluster for the antitumor angucycline oviedomycin in Streptomyces antibioticus ATCC 11891. ChemBioChem 5: 1181-1187.
22. Maehr H, Liu CM, Liu M, Perrotta A, Smallheer JM, Williams TH & Blount JF (1982) Microbial products. VI Five novel metabolites related to benz [a] anthracene from an unidentified actinomycete designated X-14881. J Antibiot 35: 1627-1631.
23. Martín MF & Liras P (1989) Organization and expression of genes involved in the biosynthesis of antibiotics and other secondary metabolites. Annu Rev Microbiol 43: 173-206.
24. McAlpine JB, Bachmann BO, Piraee M, Tremblay S, Alarco AM, Zazopoulos E & Farnet CM (2005) Microbial genomics as a guide to drug discovery and structural elucidation: ECO-02301, a novel antifungal agent, as an example. J Nat Prod 68: 493-496.
25. Metsä-Ketelä M, Halo L, Munukka E, Hakala J, Mäntsälä P & Ylihonko K (2002) Molecular evolution of aromatic polyketides and comparative sequence analysis of polyketide ketosynthase and 16S ribosomal DNA genes from various Streptomyces species. Appl Environ Microbiol 68: 4472-4479.
26. Metsä-Ketelä M, Ylihonko K & Mäntsälä P (2004) Partial activation of a silent angucycline-type gene cluster from a rubromycin β producing Streptomyces sp. PGA64. J Antibiot 57: 502-510.
27. Miller ED, Kauffman CA, Jensen PR & Fenical W (2007) Piperazimycins: cytotoxic hexadepsipeptides from a marine-derived bacterium of the genus Streptomyces. J Org Chem 72: 323-330.
28. Monaghan RL & Tkacz JS (1990) Bioactive microbial products: focus upon mechanism of action. Annu Rev Microbiol 44: 271-301.
29. Moore BS, Trischman JA, Seng D, Kho D, Jensen PR & Fenical W (1999) Salinamides, antiinflammatory depsipeptides from a marine streptomycete. J Org Chem 64: 1145-1150.
30. Ohnishi Y, Ishikawa J, Hara H et al. (2008) Genome sequence of the streptomycin-producing microorganism Streptomyces griseus IFO 13350. J Bacteriol 190: 4050-4060.
31. Ōmura S, Ikeda H, Ishikawa J et al. (2001) Genome sequence of an industrial microorganism Streptomyces avermitilis: deducing the ability of producing secondary metabolites. P Natl Acad Sci USA 98: 12215-12220.
32. Pullan ST, Chandra G, Bibb MJ & Merrick M (2011) Genome-wide analysis of the role of GlnR in Streptomyces venezuelae provides new insights into global nitrogen regulation in actinomycetes. BMC Genomics 12: 175.
33. Qin S, Zhang H, Li F, Zhu B & Zheng H (2012) Draft genome sequence of marine Streptomyces sp. strain W007, which produces angucyclinone antibiotics with a benz [a] anthracene skeleton. J Bacteriol 194: 1628-1629.
34. Ramos JL, Martinez-Bueno M, Molina-Henares AJ et al. (2005) The TetR family of transcriptional repressors. Microbiol Mol Biol Rev 69: 326-356.
35. Rees DC, Johnson E & Lewinson O (2009) ABC transporters: the power to change. Nat Rev Mol Cell Biol 10: 218-227.
36. Shen B (2003) Polyketide biosynthesis beyond the type I, II and III polyketide synthase paradigms. Curr Opin Chem Biol 7: 285-295.
37. Shen B, Du L, Sanchez C, Edwards DJ, Chen M & Murrell JM (2001) The biosynthetic gene cluster for the anticancer drug bleomycin from Streptomyces verticillus ATCC15003 as a model for hybrid peptide-polyketide natural product biosynthesis. J Ind Microbiol Biotechnol 27: 378-385.
38. Shigihara Y, Koizumi Y, Tamamura T et al. (1988) 6-deoxy-8-O-methylrabelomycin and 8-O-methylrabelomycin from a Streptomyces species. J Antibiot 41: 1260-1264.
39. Solanki R, Khanna M & Lal R (2008) Bioactive compounds from marine actinomycetes. Indian J Microbiol 48: 410-431.
40. Staunton J & Wilkinson B (2001) Combinatorial biosynthesis of polyketides and nonribosomal peptides. Curr Opin Chem Biol 5: 159-164.
41. Sujatha P, Bapi Raju KVVSN & Ramana T (2005) Studies on a new marine streptomycete BT-408 producing polyketide antibiotic SBR-22 effective against methicillin resistant Staphylococcus aureus. Microbiol Res 160: 119-126.
42. Udwary DW, Gontang EA, Jones AC et al. (2011) Significant natural product biosynthetic potential of actinorhizal symbionts of the genus Frankia, as revealed by comparative genomic and proteomic analyses. Appl Environ Microbiol 77: 3617-3625.
43. Wang H, Li H, Zuo M, Zhang Y, Liu H, Fang W & Chen X (2008) Lx2-32c, a novel taxane and its antitumor activities in vitro and in vivo. Cancer Lett 268: 89-97.
44. Wang H, Ma X, Ren S, Buolamwini JK & Yan C (2011) A small-molecule inhibitor of MDMX activates p53 and induces apoptosis. Mol Cancer Ther 10: 69-79.
45. Xie Z, Liu B, Wang H et al. (2012) Kiamycin, a unique cytotoxic angucyclinone derivative from a marine Streptomyces sp. Mar Drugs 10: 551-558.
46. Zazopoulos E, Huang K, Staffa A et al. (2003) A genomics-guided approach for discovering and expressing cryptic metabolic pathways. Nat Biotechnol 21: 187-190.
47. Zeng LR & Xie JP (2011) Molecular basis underlying LuxR family transcription factors and function diversity and implications for novel antibiotic drug targets. J Cell Biochem 112: 3079-3084.
48. Zhang H, Wang H, Cui H et al. (2011) A new anthracene derivative from marine Streptomyces sp. W007 exhibiting highly and selectively cytotoxic activities. Mar Drugs 9: 1502-1509.