Natural variation in the microcystin synthetase operon mcyABC and impact on microcystin production in Microcystis strains

Journal of Bacteriology

Volumn 185, Issue 9, 2003, Pages 2774-2785

  Mikalsen, Bjørg ^a   Boison, Gudrun ^d   Skulberg, Olav M ^b   Fastner, Jutta ^e   Davies, William ^a   Gabrielsen, Tove M ^a   Rudi, Knut ^c   Jakobsen, Kjetill S ^a  

^a UNIVERSITY OF OSLO   (Norway)

^b NORWEGIAN INSTITUTE FOR WATER RESEARCH   (Norway)

^c NORWEGIAN FOOD RESEARCH INSTITUTE   (Norway)

^d UNIVERSITY OF COLOGNE   (Germany)

^e TECHNISCHE UNIVERSITÄT BERLIN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CYANOGINOSIN; DNA 16S; MICROCYSTIN SYNTHETASE; SYNTHETASE; UNCLASSIFIED DRUG;

ADENYLATION; ARTICLE; BACTERIAL GENE; BACTERIAL STRAIN; CORRELATION ANALYSIS; DNA FINGERPRINTING; ENZYME SPECIFICITY; GENE CLUSTER; GENE LOSS; GENE SEQUENCE; GENE TRANSFER; GENETIC VARIABILITY; MCYABC GENE; MCYB1 GENE; MICROCYSTIS; NONHUMAN; NUCLEOTIDE SEQUENCE; OPERON; PHYLOGENY; PRIORITY JOURNAL; PROTEIN DOMAIN;

AMINO ACID SEQUENCE; BACTERIAL PROTEINS; GENE DELETION; GENE TRANSFER, HORIZONTAL; GENES, BACTERIAL; MICROCYSTINS; MICROCYSTIS; MOLECULAR SEQUENCE DATA; MULTIGENE FAMILY; OPERON; PEPTIDE SYNTHASES; PEPTIDES, CYCLIC; PHYLOGENY; RECOMBINATION, GENETIC; SEQUENCE ALIGNMENT; SEQUENCE ANALYSIS; SPECIES SPECIFICITY; VARIATION (GENETICS);

BACTERIA (MICROORGANISMS); MICROCYSTIS; PROKARYOTA;

EID: 0242417422     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.185.9.2774-2785.2003     Document Type: Article

References (52)

1. An, J., and W. W. Carmichael. 1994. Use of a colorimetric protein phosphatase inhibition assay and enzyme linked immunosorbent assay for the study of microcystins and nodularins. Toxicon 32:1495-1507.
2. Arment, A. R., and W. W. Carmichael. 1996. Evidence that microcystin is a thio-template product. J. Phycol. 32:591-597.
3. Asayama, M., M. Kabasawa, I. Takahashi, T. Aida, and M. Shirai. 1996. Highly repetitive sequences and characteristics of genomic DNA in unicellular cyanobacterial strains. FEMS Microbiol. Lett. 137:175-181.
4. Baker, J. A., B. A. Neilan, B. Entsch, and D. B. McKay. 2001. Identification of cyanobacteria and their toxigenicity in environmental samples by rapid molecular analysis. Environ. Toxicol. 16:472-482.
5. Beasley, V. R., W. O. Cook, A. M. Dahlem, S. B. Hooser, R. A. Lovell, and W. M. Valentine. 1989. Algae intoxication in livestock and waterfowl. Food Anim. Pract. 5:345-361.
6. Carmichael, W. W. 1994. The toxins of cyanobacteria. Sci. Am. 270:78-86.
7. Challis, G. L., J. Ravel, and C. A. Townsend. 2000. Predictive, structure-based model of amino acid recognition by nonribosomal peptide synthetase adenylation domains. Chem. Biol. 7:211-224.
8. Conti, E., T. Stachelhaus, M. A. Marahiel, and P. Brick. 1997. Structural basis for the activation of phenylalanine in the non-ribosomal biosynthesis of gramicidin S. EMBO J. 16:4174-4183.
9. DeMott, W. R., Q. X. Zhang, and W. W. Carmichael. 1991. Effects of toxic cyanobacteria and purified toxins on the survival and feeding of a copepod and three species of Daphnia. Limnol. Oceanogr. 36:1346-1357.
10. Dittmann, E., M. Erhard, M. Kaebernick, C. Scheler, B. A. Neilan, H. von Döhren, and T. Börner. 2001. Altered expression of two light-dependent genes in a microcystin-lacking mutant of Microcystis aeruginosa PCC 7806. Microbiology 147:3113-3119.
11. Dittmann, E., B. A. Neilan, M. Erhard, H. von Döhren, and T. Börner. 1997. Insertional mutagenesis of a peptide synthetase gene that is responsible for hepatotoxin production in the cyanobacterium Microcystis aeruginosa PCC 7806. Mol. Microbiol. 26:779-787.
12. Erhard, M., H. von Döhren, and P. Jungblut. 1997. Rapid typing and elucidation of new secondary metabolites of intact cyanobacteria using MALDITOF mass spectrometry. Nat. Biotechnol. 15:906-909.
13. Eriksson, J. E., L. Gronberg, S. Nygard, J. P. Slotte, and J. A. Meriluoto. 1990. Hepatocellular uptake of 3H-dihydromicrocystin-LR, a cyclic peptide toxin. Biochim. Biophys. Acta 1025:60-66.
14. Eriksson, J. E., D. Toivola, J. A. Meriluoto, H. Karaki, Y. G. Han, and D. Hartshorne. 1990. Hepatocyte deformation induced by cyanobacterial toxins reflects inhibition of protein phosphatases. Biochem. Biophys. Res. Commun. 173:1347-1353.
15. Espelund, M., R. A. Stacy, and K. S. Jakobsen. 1990. A simple method for generating single-stranded DNA probes labeled to high activities. Nucleic Acids Res. 18:6157-6158.
16. Fastner, J., M. Erhard, W. W. Carmichael, F. Sun, K. L. Rinehart, H. Ronicke, and I. Chorus. 1999. Characterization and diversity of microcystins in natural blooms and strains of the genera Microcystis and Planktothrix from German freshwaters. Arch. Hydrobiol. 145:147-163.
17. Felsenstein, J. 1985. Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783-791.
18. Galau, G. A., D. W. Hughes, and L. Dure III. 1986. Abscisic acid induction of cloned cotton late embryogenesis-abundant (Lea) mRNAs. Plant Mol. Biol. 7:155-177.
19. Holmes, E. C., M. Worobey, and A. Rambaut. 1999. Phylogenetic evidence for recombination in dengue virus. Mol. Biol. Evol. 16:405-409.
20. Honkanen, R. E., J. Zwiller, R. E. Moore, S. L. Daily, B. S. Khatra, M. Dukelow, and A. L. Boynton. 1990. Characterization of microcystin-LR, a potent inhibitor of type 1 and type 2A protein phosphatases. J. Biol. Chem. 265:19401-19404.
21. Jochimsen, E. M., W. W. Carmichael, J. S. An, D. M. Cardo, S. T. Cookson, C. E. Holmes, M. B. Antunes, D. A. de Melo Filho, T. M. Lyra, V. S. Barreto, S. M. Azevedo, and W. R. Jarvis. 1998. Liver failure and death after exposure to microcystins at a hemodialysis center in Brazil. N. Engl. J. Med. 338:873-878.
22. Kaebernick, M., E. Dittmann, T. Borner, and B. A. Neilan. 2002. Multiple alternate transcripts direct the biosynthesis of microcystin, a cyanobacterial nonribosomal peptide. Appl. Environ. Microbiol. 68:449-455.
23. Kimura, M. 1980. A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J. Mol. Evol. 16:111-120.
24. Kleinkauf, H., and H. von Döhren. 1996. A nonribosomal system of peptide biosynthesis. Eur. J. Biochem. 236:335-351.
25. Krätzschmar, J., M. Krause, and M. A. Marahiel. 1989. Gramicidin S biosynthesis operon containing the strucural genes grsA and grsB has an open reading frame encoding a protein homologous to fatty acid thioesterases. J. Bacteriol. 171:5422-5429.
26. Kurmayer, R., E. Dittmann, J. Fastner, and I. Chorus. 2002, Diversity of microcystin genes within a population of the toxic cyanobacterium Microcystis spp. in Lake Wannsee (Berlin, Germany). Microb. Ecol. 43:107-118.
27. Lichtenstein, C. P., and J. Draper. 1985. Genetic engineering of plants, p. 67-119. In D. M. Glover (ed.), DNA cloning: a practical approach, vol. 2. IRL Press, Oxford, United Kingdom.
28. MacKintosh, C., K. A. Beattie, S. Klumpp, P. Cohen, and G. A. Codd. 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.
29. Maddison, W. P., and D. R. Maddison. 1989. Interactive analysis of phylogeny and character evolution using the computer-program MacClade. Folia Primatol. 53:190-202.
30. Marahiel, M. A., T. Stachelhaus, and H. D. Mootz. 1997. Modular peptide synthetases involved in nonribosomal peptide synthesis. Chem. Rev. 97:2651-2673.
31. Meissner, K., E. Dittmann, and T. Börner. 1996. Toxic and non-toxic strains of the cyanobacterium Microcystis aeruginosa contain sequences homologous to peptide synthetase genes. FEMS Microbiol. Lett. 135:295-303.
32. Metcalf, J. S., S. G. Bell, and G. A. Codd. 2000. Production of novel polyclonal antibodies against the cyanobacterial toxin microcystin-LR and their application for the detection and quantification of microcystins and nodularin. Water Res. 34:2761-2769.
33. Neilan, B. A. 1995. Identification and phylogenetic analysis of toxigenic cyanobacteria by multiplex randomly amplified polymorphic DNA PCR. Appl. Environ. Microbiol. 61:2286-2291.
34. Neilan, B. A., D. Jacobs, T. Del Dot, L. L. Blackall, P. R. Hawkins, P. T. Cox, and A. E. Goodman. 1997. rRNA sequences and evolutionary relationships among toxic and nontoxic cyanobacteria of the genus Microcystis. Int. J. Syst. Bacteriol. 47:693-697.
35. Nishihara, H., H. Miwa, M. Watanabe, M. Nagashima, O. Yagi, and Y. Takamura. 1997. Random amplified polymorphic DNA (RAPD) analyses for discriminating genotypes of Microcystis cyanobacteria. Biosci. Biotechnol. Biochem. 61:1067-1072.
36. Nishizawa, T., A. Ueda, M. Asayama, K. Fujii, K. Harada, K. Ochi, and M. Shirai. 2000. Polyketide synthase gene coupled to the peptide synthetase module involved in the biosynthesis of the cyclic heptapeptide microcystin. J. Biochem. 127:779-789.
37. Otsuka, S., S. Suda, R. H. Li, M. Watanabe, H. Oyaizu, S. Matsumoto, and M. M. Watanabe. 1998. 16S rDNA sequences and phylogenetic analyses of Microcystis strains with and without phycoerythrin. FEMS Microbiol. Lett. 164:119-124.
38. Rohlf, F. J. 2000. NTSYS-PC. Numerical taxonomy and multivariate analysis system, 2.1 ed. Exeter Software, Setauket, N.Y.
39. Rouhiainen, L., K. Sivonen, W. J. Buikema, and R. Haselkorn. 1995. Characterization of toxin-producing cyanobacteria by using an oligonucleotide probe containing a tandemly repeated heptamer. J. Bacteriol. 177:6021-6026.
40. Leu(UAA) group I intron by both horizontal intron transfer and recombination of the entire tRNA locus. J. Bacteriol. 184:666-671.
41. Leu group I introns in cyanobacterial radiation. J. Bacteriol. 181: 3445-3451. (Erratum, 182:1457, 2000.)
42. Rudi, K., and K. S. Jakobsen. 1997. Cyanobacterial tRNA(Leu)(UAA) group I introns have polyphyletic origin. FEMS Microbiol Lett. 156:293-298.
43. Rudi, K., O. M. Skulberg, and K. S. Jakobsen. 1998. Evolution of cyanobacteria by exchange of genetic material among phyletically related strains. J. Bacteriol. 180:3453-3461.
44. Rudi, K., O. M. Skulberg, F. Larsen, and K. S. Jakobsen. 1997. Strain characterization and classification of oxyphotobacteria in clone cultures on the basis of 16S rRNA sequences from the variable regions V6, V7, and V8. Appl. Environ. Microbiol. 63:2593-2599.
45. Skulberg, R., and O. M. Skulberg. 1990. Research with algal cultures. NIVA's Culture Collection of Algae. Norwegian Institute for Water Research, Oslo, Norway.
46. Stachelhaus, T., H. D. Mootz, and M. A. Marahiel. 1999. The specificity-conferring code of adenylation domains in nonribosomal peptide synthetases. Chem. Biol. 6:493-505.
47. Swofford, D. L. 2002. PAUP*. Phylogenetic analyses using parsimony (*and other methods), 4.0b ed. Sinauer Associates, Sunderland, Mass.
48. Thompson, J. D., T. J. Gibson, F. Plewniak, F. Jeanmougin, and D. G. Higgins. 1997. The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 25:4876-4882.
49. Tillett, D., E. Dittmann, M. Erhard, H. von Döhren, T. Börner, and B. A. Neilan. 2000. Structural organization of microcystin biosynthesis in Microcystis aeruginosa PCC7806: an integrated peptide-polyketide synthetase system. Chem. Biol. 7:753-764.
50. Tillett, D., D. L. Parker, and B. A. Neilan. 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.
51. Utkilen, H., and N. Gjølme. 1995. Iron-stimulated toxin production in Microcystis aeruginosa. Appl. Environ. Microbiol. 61:797-800.
52. Versalovic, J., T. Koeuth, and J. R. Lupski. 1991. Distribution of repetitive DNA sequences in eubacteria and application to fingerprinting of bacterial genomes. Nucleic Acids Res. 19:6823-6831.