Genetic analysis of the microcystin biosynthesis gene cluster in Microcystis strains from four bodies of eutrophic water in Japan

Journal of General and Applied Microbiology

Volumn 55, Issue 2, 2009, Pages 111-123

  Noguchi, Takahiko ^a,b   Shinohara, Azusa ^b   Nishizawa, Akito ^b   Asayama, Munehiko ^b   Nakano, Tomoyo ^c   Hasegawa, Masateru ^b   Harada, Ken Ichi ^c   Nichizawa, Tomoyasu ^b   Shirai, Makoto ^b  

^a Koibuchi College of Agriculture and Nutrition   (Japan)

^b IBARAKI UNIVERSITY   (Japan)

^c MEIJO UNIVERSITY   (Japan)

Author keywords

16S 23S rRNA gene ITS sequence; Cyanobacteria; McyI dehydrogenase activity; Microcystin biosynthesis gene; Microcystis

Indexed keywords

INTERNAL TRANSCRIBED SPACER; MICROCYSTIN; MICROCYSTIN A; MICROCYSTIN C; MICROCYSTIN D; MICROCYSTIN J; UNCLASSIFIED DRUG;

AMPLICON; ARTICLE; BACTERIAL GENE; BACTERIAL GENETICS; BACTERIAL STRAIN; CONTROLLED STUDY; EUTROPHICATION; GENE CLUSTER; GENE DELETION; GENE LOCUS; GENETIC ANALYSIS; GENETIC TRANSCRIPTION; GEOGRAPHY; JAPAN; MICROCYSTIS; MOLECULAR PHYLOGENY; NONHUMAN; NUCLEOTIDE SEQUENCE;

BACTERIAL PROTEINS; BASE SEQUENCE; DNA, RIBOSOMAL SPACER; GENE EXPRESSION REGULATION, BACTERIAL; GENE ORDER; GENES, BACTERIAL; JAPAN; MICROCYSTINS; MICROCYSTIS; MOLECULAR SEQUENCE DATA; MULTIGENE FAMILY; PEPTIDE SYNTHASES; PHYLOGENY; WATER MICROBIOLOGY;

CYANOBACTERIA; MICROCYSTIS;

EID: 67649200496     PISSN: 00221260     EISSN: 13498037     Source Type: Journal    
DOI: 10.2323/jgam.55.111     Document Type: Article

References (47)

1. Asayama, M., Kabasawa, M., Takahashi, I., Aida, T., and Shirai, M. (1996) Highly repetitive sequences and characteristics of genomic DNA in unicellular cyanobacterial strains. FEMS Microbiol. Lett., 137, 175-181.
2. Carmichael, W. W. (1994) The toxins of cyanobacteria. Sci. Am., 270, 78-86.
3. 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.
4. Christiansen, G., Kurmayer, R., Liu, Q., and Börner, T. (2006) Transposon inactivate biosynthesis of the nonribosomal peptide microcystin in naturally occurring Planktothrix spp. Appl. Environ. Microbiol., 72, 117-123.
5. Christiansen, G., Molitor, C., Philmus, B., and Kurmayer, R. (2008) Nontoxic strains of cyanobacteria are the result of major gene deletion events induced by a transposable element Mol. Biol. Evol., 25, 1695-1704.
6. Finking, R. and Marahiel, M. A. (2004) Biosynthesis of nonribosomal peptides 1. Annu. Rev. Microbiol., 58, 453-488.
7. Frangeul, L., Quillardet, P., Castets, A. M., Humbert, J. F., Matthijs, H. C., Cortez, D., Tolonen, A., Zhang, C. C., Gribaldo, S., Kehr, J. C., Zilliges, Y., Ziemert, N., Becker, S., Talla, E., Latifi, A., Billault, A., Lepelletier, A., Dittmann, E., Bouchier, C., and de Marsac, N. T. (2008) Highly plastic genome of Microcystis aeruginosa PCC 7806, a ubiquitous toxic fresh-water cyanobacterium. BMC Genomics, 9, 274.
8. Harada, K.-I., 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.
9. Harada, K.-I., Ogawa, K., Matsuura, K., Nagai, H., Murata, H., Suzuki, M., Itezono, Y., Nakayama, N., Shirai, M., and Na kano, M. (1991) Isolation of two toxic heptapeptide microcystins from an axenic strain of Microcystis aeruginosa K-139. Toxicon, 29, 479-489.
10. Hotto, A. M., Satchwell, M. F., and Boyer, G. L. (2007) Molecular characterization of potential microcystin-producing cyanobacteria in Lake Ontario Embayments and nearshore waters. Appl. Environ. Microbiol., 73, 4570-4578.
11. Jochimsen, E. M., Carmichael, W. W., An, J. S., Cardo, D. M., Cookson, S. T., Holmes, C. E., Antunes, M. B., Filho, D. A. M., Lyra, T. M., Barreto, V. S., Azevedo, S. M., and Jarvis, W. R. (1998) Liver failure and death after exposure to microcystins at a hemodialysis center in Brazil. N. Engl. J. Med., 338, 873-878.
12. Kaebernick, M., Dittmann, E., Börner, T., and Neilan, B. A. (2002) Multiple alternate transcripts direct biosynthesis of microcystin, a cyanobacterial nonribosomal peptide. Appl. Environ. Microbiol., 68, 449-455.
13. Kaneko, T., Nakajima, N., Okamoto, S., Suzuki, I., Tanabe, Y., Tamaoki, M., Nakamura, Y., Kasai, F., Watanabe, A., Kawashima, K., Kishida, Y., Ono, A., Shimizu, Y., Takahashi, C., Minami, C., Fujishiro, T., Kohara, M., Katoh, M., Nakazaki, N., Nakayama, S., Yamada, M., Tabata, S., and Watanabe, M. M. (2007) Complete genomic structure of the bloom-forming toxic cyanobacterium Microcystis aeruginosa NIES-843. DNA Res., 14, 247-256.
14. Lu, W., Evans, H., McColl, S. M., and Saunders, V. A. (1997) Identification of cyanobacteria by polymorphisms of PCR-amplified ribosomal DNA spacer region. FEMS Microbiol. Lett., 153, 141-149.
15. MacKintosh, C., Beattie, K. A., Klumpp, S., Cohen, P., and Codd, G. A. (1990) Cyanobacterial microcystin-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. Matsui, M., Yoshimura, T., Wakabayashi, Y., Imamura, S., Tanaka, K., Takahashi, H., Asayama, M., and Shirai, M. (2007) Interference expression at levels of the transcript and pro tein among group 1, 2, and 3 sigma factor genes in cyanobacterium. Microbes Environ., 22, 32-43.
18. Matsunaga, H., Harada, K.-I., Senma, M., Ito, Y., Yasuda, N., Ushida, S., and Kimura, Y. (1999) Possible cause of unnatural mass death of wild birds in a pond in Nishinomiya, Japan: Sudden appearance of toxic cyanobacteria. Natural Toxins, 7, 81-84.
19. Mbedi, S., Welker, M., Fastner, J., and Wiedner, C. (2005) Variability of the microcystin synthetase gene cluster in the ge nus Planktothrix (Oscillatoriales, Cyanobacteria). FEMS Microbiol. Lett., 245, 299-306.
20. Mez, K., Beattie, K. A., Codd, G. A., Hanselmann, K., and Hauser, B. (1997) Identification of a microcystin in benthic cyanobacteria linked to cattle deaths on alpine pastures in Switzerland. Eur. J. Phycol., 32, 111-117.
21. Mikalsen, B., Boison, G., Skulberg, O. M., Fastner, J., Davices, W., Gabrielsen, T. M., Rudi, K., and Jakobsen, K. S. (2003) Natural variation in the microcystin synthetase operon mcyABC and impact on microcystin production in Microcystis strains. J. Bacteriol., 185, 2774-2785.
22. Neilan, B. A., Jacobs, D., Del Dot, T., Blackall, L. L., Hawkins, P. R., Cox, P. T., and Goodman, A. E. (1997) rRNA sequences and evolutionary relationships among toxic and nontoxic cyanobacteria of the genus Microcystis. Int. J. Syst. Bacteriol., 47, 693-697.
23. Nishiwaki-Matsushima, R., Ohta, T., Nishiwaki, S., Suganuma, M., Kohyama, K., Ishikawa, T., Carmichael, W. W., and Fujiki, H. (1992) Liver tumor promotion by the cyanobacterial cyclic peptide toxin microcystin-LR. J. Cancer Res. Clin. Oncol., 118, 420-421.
24. Nishizawa, A., Arshad, A. B., Nishizawa, T., Asayama, M., Fujii, K., Nakano, T., Harada, K.-I., and Shirai, M. (2007) Cloning and characterization of a new hetero-gene cluster of nonribosomal peptide synthetase and polyketide synthase from the cyanobacterium Microcystis aeruginosa K-139. J. Gen. Appl. Microbiol., 53, 17-27.
25. Nishizawa, T. (2001) Genetic analysis of the non-ribosomal peptide synthetase genes for a cyclic-peptide microcystin in Microcystis spp. Doctoral Thesis, Dissertation in Tokyo University of Agriculture and Technology (In Japanese).
26. Nishizawa, T., Asayama, M., Fujii, K., Harada, K.-I., and Shirai, M. (1999) Genetic analysis of the peptide synthetase genes for a cyclic heptapeptide microcystin in Microcystis spp. J. Biochem., 126, 520-529.
27. Nishizawa, T., Asayama, M., and Shirai, M. (2001) Cyclic heptapeptide microcystin biosynthesis requires the glutamate racemase gene. Microbiology, 147, 1235-1241.
28. Nishizawa, T., Nishizawa, A., Asayama, M., Harada, K.-I., and Shirai, M. (2007) Diversity within the microcystin biosynthetic gene clusters among the genus Microcystis. Microbes Environ., 22, 380-390.
29. Nishizawa, T., Ueda, A., Asayama, M., Fujii, K., Harada, K.-I., Ochi, 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.
30. Otsuka, S., Suda, S., Li, R., Watanabe, M., Oyaizu, H., Matsumoto, S., and Watanabe, M. M. (1999) Phylogenetic relationships between toxic and non-toxic strains of the genus Microcystis based on 16S to 23S internal transcribed spacer sequence. FEMS Microbiol. Lett., 172, 15-21.
31. Pearson, L. A., Barrow, K. D., and Neilan, B. A. (2007) Characterization of the 2-hydroxy-acid dehydrogenase McyI, en coded within the microcystin biosynthesis gene cluster of Microcystis aeruginosa PCC7806. J. Biol. Chem., 282, 4681-4692.
32. Pearson, L. A., Hisbergues, M., Börner, T., Dittmann, E., and Neilan, B. A. (2004) Inactivation of an ABC transporter gene, mcyH, results in loss of microcystin production in the cyanobacterium Microcystis aeruginosa PCC 7806. Appl. Environ. Microbiol., 70, 6370-6378.
33. Rantala, A., Fewer, D. P., Hisbergues, M., Rouhiainen, L., Vaitomaa, J., Börner, T., and Sivonen, K. (2004) Phylogenetic evidence for the early evolution of microcystin synthesis. Proc. Natl. Acad. Sci. USA, 101, 568-573.
34. Rantala, A., Rajaniemi-Wacklin, P., Lyra, C., Rintala, J., Mankiewicz-Boczek, J. J., and Sivonen, K. (2006) Detection of microcystin-producing cyanobacteria in Finnish lakes with genus-specific microcystin synthetase gene E (mcyE) PCR and associations with environmental factors. Appl. Environ. Microbiol., 72, 6101-6110.
35. Rouhiainen, L., Vakkilainen, T., Siemer, S., Buikema, W., Haselkorn, R., and Sivonen, K. (2004) Genes coding for hepatotoxic heptapeptides (microcystins) in the cyanobac terium Anabaena strain 90. Appl. Environ. Microbiol., 70, 686-692.
36. Sakamoto, T., Shirai, M., Asayama, M., Aida, T., Sato, A., Tanaka, K., Takahashi, H., and Nakano, M. (1993) Characteristics of DNA and multiple rpoD homologous of Microcystis (Synechocystis) strains. Int. J. Syst. Bacteriol., 43, 844-847.
37. Sambrook, J., Fritsch, E. F., and Maniatis, M. (1989) Molecular Cloning; A Laboratory Manual, 2nd ed., Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY
38. Shirai, M., Matsumaru, K., Ohtake, 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.
39. Shirai, M., Ohtake, A., Sano, T., Matsumoto, S., Sakamoto, T., Sato, A., Aida, T., Harada, K., Shimada, T., and Suzuki, M. (1991) Toxicity and toxins of natural blooms and isolated strains of Microcystis spp. (Cyanobacteria) and improved procedure for purification of cultures. Appl. Environ. Microbiol., 57, 1241-1245.
40. Sielaff, H., Dittmann, E., de Marsac, N. T., Bouchier, C., von Döhren, H., Börner, T., and Schwecke, T. (2003) The mcyF gene of the microcystin biosynthetic gene cluster from Microcystis aeruginosa encodes and aspartate racemase. Biochem. J., 373, 909-916.
41. 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 Cho rus, I. and Bartram, J., E & FN Spoon, London, UK, pp. 41-111.
42. Thompson, J. D., Gibson, T. J., Plewniak, F., Jeanmougin, F., and Higgins, D. G. (1997) The CLUSTAL X windows interface: Flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res., 25, 4876-4882.
43. Tillett, D., Dittmann, E., Erhard, M., von Dohren, 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.
44. Tillett, D., Parker, D. L., and Neilan, B. A. (2001) Detection of toxigenicity by a probe for the microcystin synthetase a gene (mcyA) of the cyanobacterial genus Microcystis: Comparison of toxicities with 16S rRNA and phycocyanin operon (phycocyanin intergenic spacer) phylogenies. Appl. Environ. Microbiol., 67, 2810-2818.
45. Tooming-Klunderud, A., Mikalsen, B., Kristensen, T., and Jakobsen, K. S. (2008) The mosaic structure of the mcyABC aperon in Microcystis. Microbiology, 154, 1886-1899.
46. Yoshida, T., Takashima, Y., Tomaru, Y., Shirai, Y., Takao, Y., Hiroishi, S., and Nagasaki, K. (2006) Isolation and characteriza tion of a cyanophage infecting the toxic cyanobacterium Microcystis aeruginosa. Appl. Environ. Microbiol., 72, 1239-1247.
47. Yoshida, T., Yuki, Y., Lei, S., Chinen, H., Yoshida, M., Kondo, R., and Hiroishi, S. (2003) Quantitative detection of toxic strains of the cyanobacterial genus Microcystis by competitive PCR. Microbes Environ., 18, 16-23.