Direct evidence for production of microcystins by Anabaena strains from the Baltic Sea

Applied and Environmental Microbiology

Volumn 73, Issue 20, 2007, Pages 6543-6550

  Halinen, Katrianna ^a   Jokela, Jouni ^a   Fewer, David P ^a   Wahlsten, Matti ^a   Sivonen, Kaarina ^a  

^a UNIVERSITY OF HELSINKI   (Finland)

Author keywords

[No Author keywords available]

Indexed keywords

COASTAL ZONES; GENETIC ENGINEERING; PEPTIDES; SALINE WATER; TOXIC MATERIALS;

ANABAENA STRAINS; FRESHWATER BODIES; MICROCYSTINS; NEUROTOXINS;

ALGAE;

CYANOGINOSIN; CYANOGINOSIN LR; RNA 16S;

COASTAL ZONE; CYANOBACTERIUM; MORPHOLOGY; NITROGEN FIXATION; PEPTIDE; PRIMARY PRODUCTION; SALINITY; TOXIN;

ANABAENA; ARTICLE; BACTERIAL METABOLISM; BACTERIAL STRAIN; BACTERIUM ISOLATION; BALTIC SEA; FINLAND; GENE SEQUENCE; GENETIC HETEROGENEITY; NONHUMAN; NUCLEOTIDE SEQUENCE; RNA SEQUENCE; SALINITY; SEQUENCE ANALYSIS; TOXIN ANALYSIS;

ANABAENA; DNA, BACTERIAL; FINLAND; MICROCYSTINS; MOLECULAR SEQUENCE DATA; PHYLOGENY; RNA, RIBOSOMAL, 16S; SEAWATER; SEQUENCE ANALYSIS, DNA;

ATLANTIC OCEAN; BALTIC SEA; GULF OF FINLAND;

ANABAENA; ANABAENA SP.; APHANIZOMENON FLOS-AQUAE; CYANOBACTERIA; NODULARIA SPUMIGENA;

EID: 35448947193     PISSN: 00992240     EISSN: None     Source Type: Journal    
DOI: 10.1128/AEM.01377-07     Document Type: Article

References (50)

1. Baker, J. A., B. Entsch, B. A. Neilan, and D. B. McKay. 2002. Monitoring changing toxigenicity of a cyanobacterial bloom by molecular methods. Appl. Environ. Microbiol. 68:6070-6076.
2. Barker, G. L. A., A. Konopka, B. A. Handley, and P. K. Hayes. 2000. Genetic variation in Aphanizomenon (cyanobacteria) colonies from the Baltic Sea and North America. J. Phycol. 36:947-950.
3. Barker, G. L. A., P. K. Hayes, S. L. O'Mahony, P. Vacharapiyasophon, and A. E. Walsby. 1999. A molecular and phenotypic analysis of Nodularia (cyanobacteria) from the Baltic Sea. J. Phycol. 35:931-937.
4. Codd, G. A., J. Lindsay, F. M. Young, L. F. Morrison, and J. S. Metcalf. 2005. Harmful cyanobacteria: from mass mortalities to management measures, p. 1-23. In J. Huisman, H. C. P. Matthijs, and P. M. Visser (ed.), Harmful cyanobacteria. Springer, Dordrecht, The Netherlands.
5. Diehnelt, C. W., S. M. Peterman, and W. L. Budde. 2005. Liquid chromatography-tandem mass spectrometry and accurate mlz measurements of cyclic peptide cyanobacteria toxins. Trends Anal. Chem. 24:622-634.
6. Edwards, U., T. Rogall, H. Blöcker, M. Emde, and E. C. Böttger. 1989. Isolation and direct complete nucleotide determination of entire genes. Characterization of a gene coding for 16S ribosomal RNA. Nucleic Acids Res. 17:7843-7853.
7. Fergusson, K. M., and C. P. Saint. 2000. Molecular phylogeny of Anabaena circinalis and its identification in environmental samples by PCR. Appl. Environ. Microbiol. 66:4145-4148.
8. Finni, T., K. Kononen, R. Olsonen, and K. Wallström. 2001. The history of cyanobacterial blooms in the Baltic Sea. Ambio 30:172-178.
9. Fujii, K., K. Sivonen, T. Nakano, and K. Harada. 2002. Structural elucidation of cyanobacterial peptides encoded by peptide synthetase gene in Anabaena species. Tetrahedron 58:6863-6871.
10. Gkelis, S., P. Rajaniemi, E. Vardaka, M. Moustaka-Gouni, T. Lanaras, and K. Sivonen. 2005. Limnothrix redekei (Van Goor) Meffert (cyanobacteria) strains from Lake Kastoria, Greece form a separate phylogenetic group. Microb. Ecol. 49:176-182.
11. Gulledge, B. M., J. B. Aggen, H.-B. Huang, A. C. Nairn, and A. R. Chamberlin. 2002. The microcystins and nodularins: cyclic polypeptide inhibitors of PP1 and PP2A. Curr. Med. Chem. 9:1991-2003.
12. Harada, K.-I., K. Ogawa, Y. Kimura, H. Murata, M. Suzuki, P. M. Thorn, W. R. Evans, and W. W. Carmichael. 1991. Microcystins from Anabaena flos-aquae NRC 525-17. Chem. Res. Toxicol. 4:535-540.
13. HELCOM. 1984. Guidelines for the Baltic Monitoring Programme for the second stage (no. 12). Helsinki Commission, Helsinki, Finland.
14. Herfindal, L., L. Oftedal, F. Selheim, M. Wahlsten, K. Sivonen, and S. O. Døskeland. 2005. A high proportion of Baltic Sea benthic cyanobacterial isolates contain apoptogens able to induce rapid death of isolated rat hepatocytes. Toxicon 46:252-260.
15. Janse, I., W. E. A. Kardinaal, M. Meima, J. Fastner, P. M. Visser, and G. Zwart. 2004. Toxic and nontoxic Microcystis colonies in natural populations can be differentiated on the basis of rRNA gene internal transcribed spacer diversity. Appl. Environ. Microbiol. 70:3979-3987.
16. Kahru, M. 1997. Using satellites to monitor large-scale environmental change in the Baltic Sea, p. 43-61. In M. Kahru and C. W. Brown (ed.), Monitoring algal blooms: new techniques for detecting large-scale environmental change. Springer-Verlag, Berlin, Germany.
17. Karlsson, K. M., H. Kankaanpää, M. Huttunen, and J. Meriluoto. 2005. First observation of microcystin-LR in pelagic cyanobacterial blooms in the northern Baltic Sea. Harmful Algae 4:163-166.
18. Kaya, K., and M. M. Watanabe. 1990. Microcystin composition of an axenic clonal strain of Microcystis viridis and Microcystis viridis-containing water-blooms in Japanese freshwaters. J. Appl. Phycol. 2:173-178.
19. Kolmonen, E., K. Sivonen, J. Rapala, and K. Haukka. 2004. Diversity of cyanobacterial and heterotrophic bacteria in cyanobacterial blooms in Lake Joutikas, Finland. Aquat. Microb. Ecol. 36:201-211.
20. Koskenniemi, K. C. Lyra, P. Rajaniemi-Wacklin, J. Jokela, and K. Sivonen. 2007. Quantitative real-time PCR detection of toxic Nodularia cyanobacteria in the Baltic Sea. Appl. Environ. Microbiol. 73:2173-2179.
21. Kuiper-Goodman, T., I. Falconer, and J. Fitzgerald. 1999. Human health aspects, p. 113-153. In I. Chorus and J. Baltram (ed.), Toxic cyanobacteria in water: a guide to their public health consequences, monitoring, and management. E & FN Spon, London, United Kingdom.
22. Kullenberg, G. 1981. Physical oceanography, p. 135-181. In A. Voipio (ed.), The Baltic Sea. Elsevier Scientific Publishing Company, Amsterdam, The Netherlands.
23. 2-fixing cyanobacterium Aphanizomenon flos-aquae in the Baltic Sea with reference to Anabaena spp. and Nodularia spumigena. Boreal Env. Res. 10:19-30.
24. Laamanen, M., L. Forsström, and K. Sivonen. 2002. Diversity of Aphanizomenon flos-aquae (cyanobacterium) populations along a Baltic Sea salinity gradient. Appl. Environ. Microbiol. 68:5296-5303.
25. Laamanen, M. J., M. F. Gugger, J. M. Lehtimäki, K. Haukka, and K. Sivonen. 2001. Diversity of toxic and nontoxic Nodularia isolates (cyanobacteria) and filaments from the Baltic Sea. Appl. Environ. Microbiol. 67:4638-4647.
26. Lehtimäki, J., C. Lyra, S. Suomalainen, P. Sundman, L. Rouhiainen, L. Paulin, M. Salkinoja-Salonen, and K. Sivonen. 2000. Characterization of Nodularia strains, cyanobacteria from brackish water, by genotypic and phenotypic methods. Int. J. Syst. Evol. Microbiol. 50:1043-1053.
27. Lehtimäki, J., P. Moisander, K. Sivonen, and K. Kononen. 1997. Growth, nitrogen fixation, and nodularin production by two Baltic Sea cyanobacteria. Appl. Environ. Microbiol. 63:1647-1656.
28. Lepère, C., A. Wilmotte, and B. Meyer. 2000. Molecular diversity of Microcystis strains (Cyanophyceae, Chroococcales) based on 16S rRNA sequences. Syst. Geogr. Plant 70:275-283.
29. Luckas, B., J. Dahlmann, K. Erler, G. Gerdts, N. Wasmund, C. Hummert, and P. D. Hansen. 2005. Overview of key phytoplankton toxins and their recent occurrence in the North and Baltic Seas. Environ. Toxicol. 20:1-17.
30. Lyra, C., S. Suomalainen, M. Gugger, C. Vezie, P. Sundman, L. Paulin, and K. Sivonen. 2001. Molecular characterization of planktic cyanobacteria of Anabaena, Aphanizomenon, Microcystis, and Planktothrix genera. Int. J. Syst. Evol. Microbiol. 51:513-526.
31. 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.
32. Mazur, H., and M. Pliński. 2003. Nodularia spumigena blooms and the occurrence of hepatotoxin in the Gulf of Gdańsk. Oceanologia 45:305-316.
33. Namikoshi, M., K. Sivonen, W. R. Evans, W. W. Carmichael, L. Rouhiainen, R. Luukkainen, and K. L. Rinehart. 1992. Structures of three new homotyrosine-containing microcystins and a new homophenylalanine variant from Anabaena sp. strain 66. Chem. Res. Toxicol. 5:661-666.
34. Otsuka, S., S. Suda, R. Li, M. Watanabe, H. Oyaizu, S. Matsumoto, and M. M. Watanabe. 1999. Phylogenetic relationships between toxic and nontoxic strains of the genus Microcystis based on 16S and 23S internal transcribed spacer sequence. FEMS Microb. Lett. 172:15-21.
35. Rajaniemi, P., P. Hrouzek, K. Kaštovská, R. Willame, A. Rantala, L. Hoffmann, J. Komárek, and K. Sivonen. 2005. Phylogenetic and morphological evaluation of the genera Anabaena, Aphanizomenon, Trichormus and Nostoc (Nostocales, Cyanobacteria). Int. J. Syst. Evol. Microbiol. 55:11-26.
36. Rajaniemi-Wacklin, P., A. Rantala, M. A. Mugnai, S. Turicchia, S. Ventura, J. Komárková, L. Lepistö, and K. Sivonen. 2005. Correspondence between phylogeny and morphology of Snowella spp. and Woronichinia naegeliana, cyanobacteria commonly occurring in lakes. J. Phycol. 42:226-232.
37. Rapala, J., K. Sivonen, C. Lyra, and S. I. Niemelä. 1997. Variation of microcystins, cyanobacterial hepatotoxins, in Anabaena spp. as a function of growth stimuli. Appl. Environ. Microbiol. 63:2206-2212.
38. Repka, S., M. Meyerhöfer, K. von Bröckel, and K. Sivonen. 2004. Associations of cyanobacterial toxin, nodularin, with environmental factors and Zooplankton in the Baltic Sea. Microb. Ecol. 47:350-358.
39. Rinehart, K. L., M. Namikoshi, and B. W. Choi. 1994. Structure and biosynthesis of toxins from blue-green algae (cyanobacteria). J. Appl. Phycol. 6:159-176.
40. Sivonen, K., and G. Jones. 1999. Cyanobacterial toxins, p. 41-111. In I. Chorus and J. Baltram (ed.), Toxic cyanobacteria in water: a guide to their public health consequences, monitoring and management. E & FN Spon, London, United Kingdom.
41. Sivonen, K., K. Kononen, W. W. Carmichael, A. M. Dahlem, K. L. Rinehart, J. Kiviranta, and S. I. Niemelä. 1989. Occurrence of the hepatotoxic cyanobacterium Nodularia spumigena in the Baltic Sea and structure of the toxin. Appl. Environ. Microbiol. 55:1990-1995.
42. Sivonen, K., M. Namikoshi, R. Luukkainen, M. Färdig, L. Rouhiainen, W. R. Evans, W. W. Carmichael, K. L. Rinehart, and S. I. Niemelä. 1995. Variation of cyanobacterial hepatotoxins in Finland, p. 163-169. In M. Munawar and M. Luotola (ed.), The contaminants in the Nordic ecosystem: dynamics, processes and fate. Ecovision World Monograph Series. SPB Academic Publishing, Amsterdam, The Netherlands.
43. Sivonen, K., M. Namikoshi, W. R. Evans, W. W. Carmichael, F. Sun, L. Rouhiainen, R. Luukkainen, and K. L. Rinehart. 1992. Isolation and characterization of a variety of microcystins from seven strains of the cyanobacterial genus Anabaena. Appl. Environ. Microbiol. 58:2495-2500.
44. Sivonen, K., S. I. Niemelä, R. M. Niemi, L. Lepistö, T. H. Luoma, and L. A. Räsänen. 1990. Toxic cyanobacteria (blue-green algae) in Finnish fresh and coastal waters. Hydrobiologia 190:267-275.
45. Stackebrandt, E., and B. M. Goebel. 1994. Taxonomic note: a place for DNA-DNA reassociation and 16S rRNA sequence analysis in the present species definition in bacteriology. Int. J. Syst. Bacteriol. 44:846-849.
46. Stal, L. J., P. Albertano, B. Bergman, K. von Bröckel, J. R. Gallon, P. K. Hayes, K. Sivonen, and A. E. Walsby. 2003. BASIC: Baltic Sea cyanobacteria. An investigation of the structure and dynamics of water blooms of cyanobacteria in the Baltic Sea - responses to a changing environment. Continental Shelf Res. 23:1695-1714.
47. Surakka, A., L. M. Sihvonen, J. M. Lehtimäki, M. Wahlsten, P. Vuorela, and K. Sivonen. 2005. Benthic cyanobacteria from the Baltic Sea contain cytotoxic Anabaena, Nodularia, and Nostoc strains and an apoptosis-inducing Phormidium strain. Environ. Toxicol. 20:285-292.
48. Swofford, D. L. 2003. PAUP version 4b10: phylogenetic analysis using parsimony (and other methods). Sinauer Associates, Sunderland, MA.
49. ter Braak, C. J. F., and P. Šmilauer. 2002. Canoco reference manual and CanoDraw for Windows user's guide: software for canonical community ordination (version 4.5). Microcomputer Power, Ithaca, NY.
50. Tikkanen, T. 1986. Kasviplanktonopas. Suomen luonnonsuojeluliiton tuki Oy. Forssan kirjapaino, Forssa, Finland.