Microcystin production by a freshwater spring cyanobacterium of the genus Fischerella

Toxicon

Volumn 53, Issue 7-8, 2009, Pages 754-761

  Fiore, Marli Fátima ^a   Genuário, Diego Bonaldo ^a   da Silva, Caroline Souza Pamplona ^a   Shishido, Tânia Keiko ^a   Moraes, Luiz Alberto Beraldo ^a   Neto, Romeu Cantúsio ^b   Silva Stenico, Maria Estela ^a  

^a UNIVERSITY OF SÃO PAULO   (Brazil)

^b Laboratory of Microbiology   (Brazil)

Author keywords

16S rRNA gene; mcyD; Microcystins; Polyketide synthase; Stigonematales

Indexed keywords

DNA FRAGMENT; FUNGAL DNA; FUNGAL RNA; MICROCYSTIN; NODULARIN; POLYKETIDE SYNTHASE; RNA 16S; SYNTHETASE;

ANABAENA; ARTICLE; BACTERIAL STRAIN; BACTERIUM ISOLATE; BACTERIUM ISOLATION; BIOSYNTHESIS; BOOTSTRAPPING; BRAZIL; CELL CULTURE; CONTROLLED STUDY; CYANOBACTERIUM; DRY WEIGHT; ENZYME LINKED IMMUNOSORBENT ASSAY; FISCHERELLA; FUNGAL GENE; GENE SEQUENCE; GENOME ANALYSIS; GENUS; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; MASS SPECTROMETRY; MICROCYSTIS; NONHUMAN; NUCLEOTIDE SEQUENCE; OPERON; PHYLOGENY; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DOMAIN; RNA STRUCTURE; TANDEM MASS SPECTROMETRY; TIME OF FLIGHT MASS SPECTROMETRY; TOXIN ANALYSIS;

BRAZIL; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; CYANOBACTERIA; DNA, PLANT; ENZYME-LINKED IMMUNOSORBENT ASSAY; FRESH WATER; MASS SPECTROMETRY; MICROCYSTINS; PHYLOGENY; RNA, RIBOSOMAL; SPECTROMETRY, MASS, ELECTROSPRAY IONIZATION;

ANABAENA; CYANOBACTERIA; FISCHERELLA; FISCHERELLA SP.; MICROCYSTIS; MYXUS CAPENSIS; PLANKTOTHRIX; STIGONEMATALES;

EID: 67349268411     PISSN: 00410101     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.toxicon.2009.02.010     Document Type: Article

References (53)

1. Ahmadjian V. The Lichens Symbiosis (1993), John Wiley and Sons, New York
2. Allen M.B., and Arnon D.I. Studies on nitrogen-fixing blue-green algae. I. Growth and nitrogen fixation by Anabaena cylindrica Lemm. Plant Physiol. 30 (1955) 366-372
3. Anagnostidis K., and Komárek J. Modern approach to the classification system of cyanophytes. 5-Stigonematales. Algol. Stud. 59 (1990) 1-73
4. Asthana R.K., Srivastava A., Singh A.P., Deepali, Singh S.P., Nath G., Srivastava R., and Srivastava B.S. Identification of an antimicrobial entity from the cyanobacterium Fischerella sp. isolated from bark of Azadirachta indica (neem) tree. J. Appl. Phycol. 18 (2006) 33-39
5. Azevedo S.M.F.O., Carmichael W.W., Jochimsen E.M., Rinehart K.L., Lau S., Shaw G.R., and Eaglesham G.K. Human intoxication by microcystin during renal dialysis treatment in Caruaru - Brazil. Toxicology 181 (2002) 441-446
6. Beattle K.A., Kaya K., Sano T., and Codd G. Three dehydrobutyrine-containing microcystins from Nostoc. Phytochemistry 47 (1998) 1289-1292
7. Becher P.G., and Jüttner F. Insecticidal activity - a new bioactive property of the cyanobacterium Fischerella. Pol. J. Ecol. 54 (2006) 653-662
8. Beyer S., Kunze B., Silakowski B., and Müller R. Metabolic diversity in myxobacteria: identification of the myxalamid and the stigmatellin biosynthetic gene cluster of Stigmatella aurantiaca Sg a15 and a combined polyketide-(poly) peptide gene cluster from the epothilone producing strain Sorangium cellulosum So ce90. Biochim. Biophys. Acta 1445 (1999) 185-195
9. Binder A., Wilson K., and Zuber H. C-phycocyanin from the thermophilic blue-green alga Mastigocladus laminosus. Isolation, characterization and subunit composition. FEBS Lett. 20 (1972) 111-116
10. Carmichael W.W. The cyanotoxins. Adv. Bot. Res. 27 (1997) 211-256
11. Carmichael W.W. Health effects of toxin-producing cyanobacteria: the CyanoHABs. Human Ecol. Risk Assess. 7 (2001) 1393-1407
12. Christiansen G., Fastner J., Erhard M., Börner T., and Dittmann E. Microcystin biosynthesis in Planktothrix: genes, evolution and manipulation. J. Bacteriol. 185 (2003) 564-572
13. Chu F.S., Huang X., Wei R.D., and Carmichael W.W. Production and characterization of antibodies against microcystins. Appl. Environ. Microbiol. 55 (1989) 1928-1933
14. Dawson R.M. The toxicology of microcystins. Toxicon 36 (1998) 953-962
15. Dittmann E., and Börner T. Genetic contribution to the risk assessment of microcystin in the environment. Toxicol. Appl. Pharmacol. 203 (2005) 192-200
16. Duy T.N., Lam P.K.S., Shaw G.R., and Connell D.W. Toxicology and risk assessment of freshwater cyanobacterial (blue-green algal) toxins in water. Rev. Environ. Contam. Toxicol. 163 (2000) 113-186
17. Etchegaray A., Rabello E., Dieckmann R., Moon D.H., Fiore M.F., von Döhren H., Tsai S.M., and Neilan B.A. Algicide production by the filamentous cyanobacterium Fischerella sp. CENA19. J. Appl. Phycol. 16 (2004) 237-243
18. Falch B.S., König G.M., Wright A.D., Sticher O., Angerhofer C.K., Pezzuto J.M., and Bachmann H. Biological activities of cyanobacteria: evaluation of extracts and pure compounds. Planta Med. 61 (1995) 321-328
19. Fewer D.P., Rouhiainen L., Jokela J., Wahlsten M., Laakso K., Wang H., and Sivonen K. Recurrent adenylation domain replacement in the microcystin synthetase gene cluster. BMC Evol. Biol. 7 (2007) 1-11
20. Finsinger K., Scholz I., Serrano A., Morales S., Uribe-Lorio L., Mora M., Sittenfeld A., Weckesser J., and Hess W.R. Characterization of true-branching cyanobacteria from geothermal sites and hot springs of Costa Rica. Environ. Microbiol. 10 (2008) 460-473
21. Fiore M.F., Moon D.H., Tsai S.M., Lee H., and Trevors J.T. Miniprep DNA isolation from unicellular and filamentous cyanobacteria. J. Microbiol. Methods 39 (2000) 159-169
22. Fiore M.F., Neilan B.A., Copp J.N., Rodrigues J.L.M., Tsai S.M., Lee H., and Trevors J.T. Characterization of nitrogen-fixing cyanobacteria in the Brazilian Amazon floodplain. Water Res. 39 (2005) 5017-5026
23. Fiore M.F., Sant'Anna C.L., Azevedo M.T.P., Komárek J., Kaštovský J., Sulek J., and Lorenzi A.S. The cyanobacterial genus Brasilonema, gen. nov., a molecular and phenotypic evaluation. J. Phycol. 43 (2007) 789-798
24. Hagmann L., and Jüttner F. Fischerellin A, a novel photosystem-II-inhibiting allelochemical of the cyanobacterium Fischerella muscicola with antifungal and herbicidal activity. Tetrahedron Lett. 37 (1996) 6539-6542
25. Hoffmann L., and Castenholz R.W. Subsection V (Formerly Stigonematales Geitler 1925). In: Boone D.R., and Castenholz R.W. (Eds). Bergey's Manual of Systematic Bacteriology. second ed. vol. 1 (2001), Springer, New York 589-599
26. Honkanen R.E., Caplan F.R., Baker K.K., Baldwin C.L., Bobzin S.C., Bolis C.M., Cabrera G.M., Johnson L.A., Jung J.H., Larsen L.K., Levine I.A., Moore R.E., Nelson C.S., Patterson G.M.L., Tschappat K.D., Tuang G.D., Boynton A.L., Arment A.R., An J., Carmichael W.W., Rodland K.D., Magun B.E., and Lewin R.A. Protein phosphatase inhibitory activity in extracts of cultured blue-green algae (cyanophyte). J. Phycol. 31 (1995) 478-486
27. Imanishi S., Kato H., Mizuno M., Tsuji K., and Harada K. Bacterial degradation of microcystins and nodularin. Chem. Res. Toxicol. 18 (2005) 591-598
28. Izaguirre G., Jungblut A.-D., and Neilan B.A. Benthic cyanobacteria (Oscillatoriaceae) that produce microcystin-LR, isolated from four reservoirs in southern California. Water Res. 41 (2007) 492-498
29. Kaštovský J., and Johansen J.R. Mastigocladus laminosus (Stigonematales, Cyanobacteria): phylogenetic relationship of strains from thermal spring to soil-inhabiting genera of the order and taxonomic implications for the genus. Phycologia 47 (2008) 307-320
30. Komárek J., and Hauer T. CyanoDB.cz - on-line database of cyanobacterial genera. Available from: (2004). http://www.cyanodb.cz
31. Kuiper-Goodman T., Falconer I.R., and Fitzgerald D.J. Human health aspects. In: Chorus I., and Bartram J. (Eds). Toxic Cyanobacteria in Water: a Guide to Their Public Health Consequences, Monitoring, and Management (1999), E & FN Spon, London 113-153
32. Kumar S., Tamura K., and Nei M. MEGA3: integrated software for molecular evolutionary genetics analysis and sequence alignment. Brief Bioinform. 5 (2004) 150-163
33. Lawrence J.F., Niedzwiadek B., Menard C., Lau B.P., Lewis D., Kuper-Goodman T., Carbone S., and Holmes C. Comparison of liquid chromatography/mass spectrometry, ELISA, and phosphatase assay for the determination of microcystins in blue-green algae products. J. AOAC Int. 84 (2001) 1035-1044
34. Mankiewicz-Boczek J., Izydorczyk K., Romanowska-Duda Z., Jurczak T., Stefaniak K., and Kokocinski M. Detection and monitoring toxigenicity of cyanobacteria by application of molecular methods. Environ. Toxicol. 21 (2006) 380-387
35. Mitra A.K. The algal flora of certain Indian soils. Indian J. Agric. Sci. 21 (1951) 357-373
36. Moffitt M.C., and Neilan B.A. Characterization of the nodularin synthetase gene cluster and proposed theory of the evolution of cyanobacterial hepatotoxins. Appl. Environ. Microbiol. 70 (2004) 6353-6362
37. Namikoshi M., Rinehard K.L., Sakai R., Sivonen K., and Carmichael W.W. Structures of three new cyclic heptapeptide hepatotoxins produced by the cyanobacterium (blue-green alga) Nostoc sp. strain 152. J. Org. Chem. 55 (1990) 6135-6139
38. Oksanen I., Jokela J., Fewer D.P., Wahlsten M., Rikkinen J., and Sivonen K. Discovery of rare and highly toxic microcystins from lichen-associated cyanobacterium Nostoc sp. strain IO-102-I. Appl. Environ. Microbiol. 70 (2004) 5756-5763
39. Oliveira A.C.R., Magalhães V.F., Soares R.M., and Azevedo S.M.F.O. Influence of drinking water composition on quantitation and biological activity of dissolved microcystin (cyanotoxin). Environ. Toxicol. 20 (2005) 126-130
40. Ouahid Y., Pérez-Silva G., and del Campo F.F. Identification of potentially toxic environmental Microcystis by individual and multiple PCR amplification of specific microcystin synthetase gene regions. Environ. Toxicol. 20 (2005) 235-242
41. Ouellette A.J.A., Handy S.M., and Wilhelm S.W. Toxic Microcystis is widespread in Lake Erie: PCR detection of toxin genes and molecular characterization of associated cyanobacterial communities. Microbial Ecol. 51 (2006) 154-165
42. Papke U., Gross E.M., and Francke W. Isolation, identification and determination of the absolute configuration of fischerellin B. A new algicide from the freshwater cyanobacterium Fischerella muscicola (Thruret.). Tetrahedron Lett. 38 (1997) 379-382
43. Park A., Moore R.E., and Patterson G.M.L. Fischerindole L, a new isonitrile from the terrestrial blue-green alga Fischerella muscicola. Tetrahedron Lett. 33 (1992) 3257-3260
44. Prinsep M.R., Caplan F.R., Moore R.E., Patterson G.M.L., Honkanen R.E., and Boynton A.L. Microcystin-LA from a blue-green alga belonging to the Stigonematales. Phytochemistry 31 (1992) 1247-1248
45. Rantala A., Fewer D., Hisbergues M., Rouhiainen L., Vaitomaa J., Börner T., and Sivonen K. Phylogenetic evidence for the early evolution of microcystin synthesis. Proc. Natl. Acad. Sci. U.S.A. 101 (2004) 568-573
46. Rippka R., Deruelles J., Waterbury J.B., Herdman M., and Stanier R.Y. Generic assignments, strain histories and properties of pure cultures of cyanobacteria. J. Gen. Microbiol. 111 (1979) 1-61
47. Rouhiainen L., Vakkilainen T., Siemer B.L., Buikema W., Haselkorn R., and Sivonen K. Genes coding for hepatotoxic heptapeptides (microcystins) in the cyanobacterium Anabaena strain 90. Appl. Environ. Microbiol. 70 (2004) 686-692
48. Silva-Stenico M.E., Cantúsio Neto R., Alves I.R., Moraes L.A.B., Shishido T.K., and Fiore M.F. Optimizing the extraction of the hepatotoxin microcystin-LR. J. Braz. Chem. Soc. 20 (2009)
49. Sivonen K., Carmichael W.W., Namikoshi M., Rinehart K.L., Dahlem A.M., and Niemela S.I. Isolation of hepatotoxic microcystin homologs from the filamentous fresh-water cyanobacterium Nostoc sp. strain152. Appl. Environ. Microbiol. 56 (1990) 2650-2657
50. Sivonen K., Namikoshi M., Evans W.R., Fardig M., Carmichael W.W., and Rinehart K.L. Three new microcystins, cyclic heptapeptide hepatotoxins, from Nostoc sp. strain 152. Chem. Res. Toxicol. 5 (1992) 464-469
51. Sivonen K., and Jones G. Cyanobacterial toxins. In: Chorus I., and Bartram J. (Eds). Toxic Cyanobacteria in Water. A Guide to Their Public Health Consequences, Monitoring and Management (1999), E & FN Spon, New York 41-111
52. Smitka T.A., Bonjouklian R., Doolin L., Jones N.D., Deeter J.B., Yoshida W.Y., Prinsep M.R., Moore R.E., and Patterson G.M.L. Ambiguine isonitriles, fungicidal hapalindole-type alkaloids from three genera of blue-green alga belonging to the Stigonemataceae. J. Org. Chem. 57 (1992) 857-861
53. Tillett D., Dittmann E., Erhard M., von Döhren H., Börner T., and Neilan B.A. Structural organization of microcystin biosynthesis in Microcystis aeruginosa PCC7806: an integrated peptide-polyketide synthetase system. Chem. Biol. 7 (2000) 753-764