Cloning and characterization of a new hetero-gene cluster of nonribosomal peptide synthetase and polyketide synthase from the cyanobacterium Microcystis aeruginosa K-139

Journal of General and Applied Microbiology

Volumn 53, Issue 1, 2007, Pages 17-27

  Nishizawa, Akito ^a   Arshad, Arizal Bin ^a   Nishizawa, Tomoyasu ^a   Asayama, Munehiko ^a   Fujii, Kiyonaga ^b   Nakano, Tomoyo ^b   Harada, Ken Ichi ^b   Shirai, Makoto ^a  

^a IBARAKI UNIVERSITY   (Japan)

^b MEIJO UNIVERSITY   (Japan)

Author keywords

Aeruginosin; Microcystis aeruginosa; Nonribosomal peptide (synthetase); Polyketide (synthase)

Indexed keywords

ACETYL COENZYME A BINDING PROTEIN LIKE PROTEIN; ACYL CARRIER PROTEIN; ADENOSINE TRIPHOSPHATE; AERUGINOSIN; ASPARTIC ACID; BACTERIAL PROTEIN; GENOMIC DNA; HALOGENASE; MICROCYSTIN; MICROPEPTIN; MICROVIRIDIN B; PEPTIDE SYNTHASE; POLYKETIDE SYNTHASE; PROTEIN PSM3; PROTEIN PSM3B; PROTEIN PSM3G; PROTEIN PSM3L; RECOMBINANT PROTEIN; TYROSINE;

ADENYLATION; ARTICLE; BACTERIAL GENETICS; BACTERIAL METABOLISM; BACTERIAL STRAIN; CONTROLLED STUDY; CYANOBACTERIUM; GENE CLUSTER; GENE DISRUPTION; GENE IDENTIFICATION; GENETIC ANALYSIS; GENETIC TRANSCRIPTION; GENOME SIZE; MICROCYSTIS AERUGINOSA; MOLECULAR CLONING; NONHUMAN; NUCLEOTIDE SEQUENCE; OPEN READING FRAME; OPERON; PROTEIN ANALYSIS; PROTEIN DOMAIN; PROTEIN SYNTHESIS; SEQUENCE ALIGNMENT; AMINO ACID SEQUENCE; CHEMISTRY; DNA SEQUENCE; ENZYMOLOGY; GENETICS; MICROCYSTIS; MOLECULAR GENETICS; MULTIGENE FAMILY;

MICROCYSTIS AERUGINOSA;

AMINO ACID SEQUENCE; BASE SEQUENCE; CLONING, MOLECULAR; MICROCYSTIS; MOLECULAR SEQUENCE DATA; MULTIGENE FAMILY; PEPTIDE SYNTHASES; POLYKETIDE SYNTHASES; SEQUENCE ANALYSIS, DNA; TRANSCRIPTION, GENETIC;

EID: 34248210095     PISSN: 00221260     EISSN: 13498037     Source Type: Journal    
DOI: 10.2323/jgam.53.17     Document Type: Article

References (38)

1. Aishwarya, V. R. (2006) Cloning and biochemical characterization of the hectochlorin biosynthetic gene cluster from the marine cyanobacterium Lyngbya majuscula. Doctoral Thesis, Dissertation in Oregon State University.
2. Becker, J. E., Moore, R. E., and Moore, B. S. (2004) Cloning, sequencing, and biochemical characterization of the nostocyclopeptide biosynthetic gene cluster: Molecular basis for imine macrocyclization. Gene, 325, 35-42.
3. Carmichael, W. W. (1994) The toxins of cyanobacteria. Sci. Am., 270, 78-86.
4. Challis, G. L., Ravel, J., and Townsend, C. A. (2000) Predictive, structure-based model of amino acid recognition by nonribosomal peptide synthetase adenylation domains. Chem. Biol., 7, 211-224.
5. Chang, Z., Flatt, P., Gerwick, W. H., Nguyen, V. A., Willis, C. L., and Sherman, D. H. (2002) The barbamide biosynthetic gene cluster: A novel marine cyanobacterial system of mixed polyketide synthase (PKS)-non-ribosomal peptide synthetase (NRPS) origin involving an unusual trichloroleucyl starter unit. Gene, 296, 235-247.
6. Christiansen, G., Fastner, J., Erhard, M., Börner, T., and Dittmann, E. (2003) Microcystin biosynthesis in Planktothrix: Genes, evolution, and manipulation. J. Bacteriol., 185, 564-572.
7. Daniel, J. E., Brian, L. M., Lisa, M. N., Kerry, M. P., Douglass, E. G., Mary, A. R., and William, H. G. (2004) Structure and biosynthesis of the Jamaicamides, new mixed polyketidepeptide neurotoxins from the marine cyanobacterium Lyngbya majuscula. Chem. Biol., 11, 817-833.
8. Finking, R. and Marahiel, M. A. (2004) Biosynthesis of nonribosomal peptides 1. Annu. Rev. Microbiol., 58, 453-488.
9. Fuma, S., Fujishima, Y., Corbell, N., D'Souza, C., Nakano, M. M., Zuber, P., and Yamane, K. (1993) Nucleotide sequence of 5′ portion of srfA that contains the region required for competence establishment in Bacillus subtilis. Nucleic Acids Res., 21, 93-97.
10. Harada, K., Nakano, T., Fujii, K., and Shirai, M. (2004) Comprehensive analysis system using liquid chromatography-mass spectrometry for the biosynthetic study of peptides produced by cyanobacteria. J. Chromatogr. A, 1033, 107-113.
11. Hoffmann, D., Hevel, J. M., Moore, R. E., and Moore, B. S. (2003) Sequence analysis and biochemical characterization of the nostopeptolide A biosynthetic rgene cluster from Nostoc sp. GSV224. Gene, 311, 171-180.
12. Ikeda, H., Ishikawa, J., Hanamoto, A., Shinose, M., Kikuchi, H., Shiba, T., Sakaki, Y., Hattori, M., and Omura, S. (2003) Complete genome sequence and comparative analysis of the industrial microorganism Streptomyces, avermitilis. Nat. Biotechnol., 21, 526-531.
13. Kaebernick, M., Dittmann, E., Borner, T., and Neilan, B. A. (2002) Multiple alternate transcripts direct the biosynthesis of microcystin, a cyanobacterial nonribosomal peptide. Appl. Environ. Microbiol., 68, 449-455.
14. Kragelund, B. B., Knudsen, J., and Poulsen, F. M. (1999) Acylcoenzyme A binding protein (ACBP). Biochim. Biophys. Acta, 1441, 150-161.
15. MacKintosh,.C., Beattie, K. A., Klumpp, S., Cohen, P., and Codd, G. A. (1990) Cyanobacterial mictocystin-LR is a potent and specific inhibitor of protein phosphatases 1 and 2A from both mammals and higher plants. FEBS Lett., 264, 187-192.
16. Marahiel, M. A. (1997) Protein templates for the biosynthesis of peptide antibiotics. Chem. Biol., 4, 561-567.
17. Nishizawa, T., Asayama, M., Fujii, K., Harada, K., and Shirai, M. (1999) Genetic analysis of the peptide synthetase genes for a cyclic heptapeptide microcystin in Microcystis spp. J. Biochem., 126, 520-529.
18. Nishizawa, T., Ueda, A., Asayama, M., Fujii, K., Harada, K., Ocni, K., and Shirai, M. (2000) Polyketide synthase gene coupled to the peptide synthetase module involved in the biosynthesis of the cyclic heptapeptide microcystin. J. Biochem., 127, 779-789.
19. Ohtake, A., Shirai, M., Aida, T., Mori, N., Harada, K., Matsuura, K., Suzuki, M., and Nakano, M. (1989) Toxicity of Microcystis species isolated from natural blooms and purification of the toxin. Appl. Environ. Microbiol., 55, 3202-3207.
20. Rantala, A., Fewer, D. P., Hisbergues, M., Rouhiainen, L., Vaitomaa, J., Borner, T., and Sivonen, K. (2004) Phylogenetic evidence for the early evolution of microcystin synthesis. Proc. Natl. Acad. Sci. USA, 101, 568-573.
21. Rohrlack, T., Christoffersen, K., Hansen, P. E., Zang, W., Czarnecki, O., Henning, M., Fastner, J., Erhard, M., Neilan, B. A., and Kaebernick, M. (2003) Isolation, characterization, and quantitative analysis of Microviridin J, a new Microcystis metabolite toxic to Daphnia. J. Chem. Ecol., 29, 1757-1770.
22. Rohrlack, T., Christoffersen, K., Kaebernick, M., and Neilan, B. A. (2004) Cyanobacterial protease inhibitor microviridin J causes a lethal molting disruption in Daphnia pulicaria. Appl. Environ. Microbiol., 70, 5047-5050.
23. Rouhiainen, L., Paulin, L., Suomalainen, S., Hyytiänen, H., Buikema, W., Haselkom, R., and Sivonen, K. (2000) Genes encoding synthetase of cyclic depsipeptides, anabaenopeptilides, in Anabaena strain 90. Mol. Microbiol., 37, 156-167.
24. Rouhiainen, L., Vakkilainen, T., Siemer, B. L., Buikema, W., Haselkom, R., and Sivonen, K. (2004) Genes coding for hepatotoxic heptapeptides (microcystins) in the cyanobacterium Anabaena strain 90. Appl. Environ. Microbiol., 70, 686-692.
25. Sakamoto, T., Shirai, M., Asayama, M., Aida, T., Sato, A., Tanaka, K., Takahashi, H., and Nakano, M. (1993) Characteristics of DNA and multiple rpoD homologs of Microcystis (Synechocystis) strains. Int. J. Syst. Bacteriol., 43, 844-847.
26. Sambrook, J., Fritsch, E. F., and Maniatis, M. (1989) Molecular Cloning; A Laboratory Manual, 2nd ed., Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
27. Shirai, M., Matsumaru, K., Ohotake, A., Takamura, Y., Aida, T., and Nakano, M. (1989) Development of a solid medium for growth and isolation of axenic Microcystis strains (cyanobacteria). Appl. Environ. Microbiol., 55, 2569-2571.
28. Simon, R. (1984) High frequency mobilization of gram-negative bacterial replicons by the in vitro constructed Tn5-Mob transposon. Mol. Gen. Genet., 196, 413-420.
29. Sivonen, K. and Jones, G. (1999) Cyanobacterial toxins. In Toxic Cyanobacteria in Water. A Guide to Their Public Health Consequences, Monitoring and Management, ed, by Chorus, I. and Bartram, J., E. & F. N. Spon 41-111, London.
30. Stachelhaus, T. and Marahiel, M. A. (1995) Modular structure of genes encoding multifunctional peptide synthetases required for non-ribosomal peptide synthesis. FEMS Microbiol. Lett., 125, 3-14.
31. Stachelhaus, T., Mootz, H. D., Bergendahl, V., and Marahel, M. A. (1998) Peptide bond formation in nonribosomal peptide biosynthesis. Catalytic role of the condensation domain. J. Biol. Chem., 273, 22773-22781.
32. Stachelhaus, T., Mootz, H. D., and Marahiel M. A. (1999) The specificity-conferring code of adenylation domains in nonribosomal peptide synthetases. Chem. Biol., 6, 493-505.
33. Stein, T. and Vaster, J. (1996) Amino acid activation and polymerization at modular multienzymes in nonribosomal peptide biosynthesis. Amino Acids, 10, 201-227.
34. Tang, L., Yoon, Y. J., Choi, C. Y., and Hutchinson, C. R. (1998) Characterization of the enzymatic domains in the modular polyketide synthase involved in rifamycin B biasynthesis by Amycolatopsis mediterranei. Gene, 216, 255-265.
35. Tillett, D., Diffmann, E., Erhard, M., von Döhren, H., Börner, T., and Neilan, B. A. (2000) Structural organization of microcystin biosynthesis in Microcystis aeruginosa PCC7806: An integrated peptide-polyketide synthetase system. Chem. Biol., 7, 753-764.
36. 2-dependent halogenase. Proc. Natl. Acad. Sci. USA, 102, 10111-10116.
37. Yoshida, K. Fujita, Y., and Ehrlich, S. D. (1999) Three asparagine synthetase genes of Bacillus subtilis. J. Bacteriol., 181, 6081-6091.
38. Zhang, J., Quigley, N. B., and Gross, D. C. (1997) Analysis of the syrP gene, which regulates syringomycin synthesis by Pseudomonas syringae pv. syringae. Appl. Environ. Microbiol., 63, 2771-2778.