Different genotypes of anatoxin-producing cyanobacteria coexist in the Tarn River, France

Applied and Environmental Microbiology

Volumn 73, Issue 23, 2007, Pages 7605-7614

  Cadel Six, Sabrina ^a   Peyraud Thomas, Caroline ^a   Brient, Luc ^b   De Marsac, Nicole Tandeau ^a   Rippka, Rosmarie ^a   Méjean, Annick ^a  

^a INSTITUT PASTEUR   (France)

^b UNIVERSITÉ DE RENNES 1   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CHROMATOGRAPHIC ANALYSIS; EXTRACTION; GAS CHROMATOGRAPHY; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; MASS SPECTROMETRY; RISK ASSESSMENT; RISK MANAGEMENT; RIVERS;

ANATOXIN; ANATOXIN-A; AQUATIC ENVIRONMENTS; BENTHIC CYANOBACTERIA; CULTURE COLLECTION; GAS CHROMATOGRAPHY - MASS SPECTROMETRY; GENETIC RELATEDNESS; MORPHOLOGICAL CHARACTERISTICS; OSCILLATORIA; TRANSCRIBED SPACER;

HEALTH RISKS;

ANATOXIN A; HOMOANATOXIN A; RIVER WATER; SPACER DNA; UNCLASSIFIED DRUG; BACTERIAL TOXIN; FUSED HETEROCYCLIC RINGS; HOMOANATOXIN-A; NEUROTOXIN; RIBOSOMAL SPACER DNA; RNA 16S; RNA 23S; TROPANE DERIVATIVE;

BIOFILM; COEXISTENCE; CYANOBACTERIUM; GENOTYPE; HEALTH RISK; MORTALITY; NEUROLOGY; TOXICITY; TOXIN; WATER QUALITY;

ARTICLE; BENTHOS; BIOFILM; CONTROLLED STUDY; CYANOBACTERIUM; FRANCE; GENOTYPE; MASS FRAGMENTOGRAPHY; MORPHOLOGY; NEUROTOXICITY; NONHUMAN; NUCLEOTIDE SEQUENCE; PHENOTYPE; PIGMENTATION; SEQUENCE ANALYSIS; TAXONOMY; ANIMAL; DNA SEQUENCE; DOG; GENETICS; GEOGRAPHY; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MICROBIOLOGY; MOLECULAR GENETICS; OSCILLATORIA; RIVER;

EURASIA; EUROPE; FRANCE; MIDI-PYRENEES; TARN RIVER; WESTERN EUROPE;

ANAGNOSTIDIS; ANIMALIA; CANIS FAMILIARIS; CYANOBACTERIA; GEITLERINEMA; OSCILLATORIA; OSCILLATORIALES; PHORMIDIUM;

ANIMALS; BACTERIAL TOXINS; BICYCLO COMPOUNDS, HETEROCYCLIC; CYANOBACTERIA; DNA, RIBOSOMAL SPACER; DOGS; FRANCE; GAS CHROMATOGRAPHY-MASS SPECTROMETRY; GENOTYPE; GEOGRAPHY; MOLECULAR SEQUENCE DATA; NEUROTOXINS; OSCILLATORIA; PHENOTYPE; RIVERS; RNA, RIBOSOMAL, 16S; RNA, RIBOSOMAL, 23S; SEQUENCE ANALYSIS, DNA; TROPANES; WATER MICROBIOLOGY;

EID: 38449105108     PISSN: 00992240     EISSN: None     Source Type: Journal    
DOI: 10.1128/AEM.01225-07     Document Type: Article

References (39)

1. Anagnostidis, K. 1989. Geitlerinema, a new genus of oscillatorialean cyanophytes. Plant Syst. Evol. 164:33-46.
2. Aráoz, R., H. O. Nghiêm, R. Rippka, N. Palibroda, N. Tandeau de Marsac, and M. Herdman. 2005. Neurotoxins in axenic oscillatorian cyanobacteria: coexistence of anatoxin-a and homoanatoxin-a determined by ligand-binding assay and GC/MS. Microbiology 151:1263-1273.
3. Baker, P. D., D. A. Steffensen, A. R. Humpage, B. C. Nicholson, I. R. Falconer, B. Lanthois, K. M. Fergusson, and C. P. Saint. 2001. Preliminary evidence of toxicity associated with the benthic cyanobacterium Phormidium in South Australia. Environ. Toxicol. 16:506-511.
4. Baurain, D., L. Renquin, S. Grubisic, P. Scheldeman, A. Belay, and A. Wilmotte. 2002. Remarkable conservation of internally transcribed spacer sequences of Arthrospira ("Spirulina") (Cyanophyceae, Cyanobacteria) strains from four continents and of recent and 30-year-old dried samples from Africa. J. Phycol. 38:384-393.
5. Boyer, S. L., J. R. Johansen, V. R. Flechtner, and G. L. Howard. 2002. Phylogeny and genetic variance in terrestrial Microcoleus (Cyanophyceae) species based on sequence analysis of the 16S rRNA gene and associated 16S-23S ITS region. J. Phycol. 38:1222-1235.
6. Castenholz, R. W., R. Rippka, M. Herdman, and A. Wilmotte. 2001. Subsection III, order Oscillatoriales (Elenkin 1934), p. 539-562. In D. R. Boone, R. W. Castenholz, and G. M. Garrity (ed.), Bergey's manual of systematic bacteriology, 2nd ed., vol. 1. The Archaea and the deeply branching and phototrophic bacteria. Springer-Verlag, New York, NY.
7. Edwards, C., K. Beattie, C. Scrimgeour, and G. Codd. 1992. Identification of anatoxin-a in benthic cyanobacteria (blue-green algae) and in associated dog poisoning at Loch Insh, Scotland. Toxicon 30:1165-1175.
8. Gugger, M., S. Lenoir, C. Berger, A. Ledreux, J. C. Druart, J. F. Humbert, C. Guette, and C. Bernard. 2005. First report in a river in France of the benthic cyanobacterium Phormidium favosum producing anatoxin-a associated with dog neurotoxicosis. Toxicon 45:919-928.
9. Gugger, M., C. Lyra, P. Henriksen, A. Couté, J. F. Humbert, and K. Sivonen. 2002. Phylogenetic comparison of the cyanobacterial genera Anabaena and Aphanizomenon. Int. J. Syst. Evol. Microbiol. 52:1867-1880.
10. Gunn, G. J., A. G. Rafferty, G. C. Rafferty, N. Cockburn, C. Edwards, K. A. Beattie, and G. A. Codd. 1992. Fatal canine neurotoxicosis attributed to blue-green algae (cyanobacteria). Vet. Rec. 130:301-302.
11. Hemscheidt, T., J. Rapala, K. Sivonen, and O. M. Skulberg. 1995. Biosynthesis of anatoxin-a in Anabaena flos-aquae and homoanatoxin-a in Oscillatoria formosa. J. Chem. Soc. Chem. Commun. 13:1361-1362.
12. Herdman, M., I. Iteman, and R. Rippka. 2005. Catalogue of cyanobacterial strains, 2nd ed. Institut Pasteur, Paris, France.
13. Iteman, I., R. Rippka, N. Tandeau de Marsac, and M. Herdman. 2000. Comparison of conserved structural and regulatory domains within divergent 16S rRNA-23S rRNA spacer sequences of cyanobacteria. Microbiology 146:1275-1286.
14. James, K. J., A. Furey, I. R. Sherlock, M. A. Stack, M. Twohig, F. B. Caudwell, and O. M. Skulberg. 1998. Sensitive determination of anatoxin-a, homoanatoxin-a and their degradation products by liquid chromatography with fluorimetric detection. J. Chromatogr. A 798:147-157.
15. Komárek, K., and K. Anagnostidis. 2005. Cyanoprokaryota. Teil 2. Oscillatoriales 19/2, p. 1-655. In B. Büdel, L. Krienitz, G. Gärtner, and M. Schagerl (ed.), Süsswasserflora von Mitteleuropa. Elsevier GmbH, München, Germany.
16. Krienitz, L., A. Ballot, K. Kotut, C. Wiegand, S. Pütz, J. Metcalf, G. Codd, and S. Pflugmacher. 2003. Contribution of hot spring cyanobacteria to the mysterious deaths of lesser flamingos at Lake Bogoria, Kenya. FEMS Microbiol. Ecol. 43:141-148.
17. Laloui, W., K. A. Palinska, R. Rippka, F. Partensky, N. Tandeau de Marsac, M. Herdman, and I. Iteman. 2002. Genotyping of axenic and non-axenic isolates of the genus Prochlorococcus and the OMF-'Synechococcus' clade by size, sequence analysis or RFLP of the internal transcribed spacer of the ribosomal operon. Microbiology 148:453-465.
18. Marquardt, J., and K. A. Palinska. 2007. Genotypic and phenotypic diversity of cyanobacteria assigned to the genus Phormidium (Oscillatoriales) from different habitats and geographical sites. Arch. Microbiol. 187:397-413.
19. Namikoshi, M., T. Murakami, M. F. Watanabe, T. Oda, J. Yamada, S. Tsujimura, H. Nagai, and S. Oishi. 2003. Simultaneous production of homoanatoxin-a, anatoxin-a, and a new non-toxic 4-hydroxyhomoanatoxin-a by the cyanobacterium Raphidiopsis mediterranea Skuja. Toxicon 42:533-538.
20. Nicholas, K. B., and H. B. Nicholas, Jr. 1997. GeneDoc: a tool for editing and annotating multiple sequence alignments. Pittsburgh Supercomputing Center, Pittsburgh, PA.
21. Onodera, H., Y. Oshima, P. Henriksen, and T. Yasumoto. 1997. Confirmation of anatoxin-a(s), in the cyanobacterium Anabaena lemmermannii, as the cause of bird kills in Danish lakes. Toxicon 35:1645-1648.
22. 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 to 23S internal transcribed spacer sequence. FEMS Microbiol. Lett. 172:15-21.
23. Otsuka, S., S. Suda, S. Shibata, H. Oyaizu, S. Matsumoto, and M. M. Watanabe. 2001. A proposal for the unification of five species of the cyanobacterial genus Microcystis Kützing ex Lemmermann 1907 under the Rules of the Bacteriological Code. Int. J. Syst. Evol. Microbiol. 51:873-879.
24. Park, H. D., K. Bomchul, K. Enkyong, and O. Tokio. 1998. Hepatotoxic microcystins, and neurotoxic anatoxin-a in cyanobacteria blooms from Korean lakes. Environ. Toxicol. Water Qual. 13:225-234.
25. Reynolds, C. S. 1991. Ecology and control of cyanobacteria (blue-green algae). Public Health Lab. Ser. Microbiol. Digest 8:87-90.
26. Rippka, R. 1988. Isolation and purification of cyanobacteria. Methods Enzymol. 167:3-27.
27. Rocap, G., D. L. Distel, J. B. Waterbury, and S. W. Chisholm. 2002. Resolution of Prochlorococcus and Synechococcus ecotypes by using 16S-23S ribosomal DNA internal transcribed spacer sequences. Appl. Environ. Microbiol. 68:1180-1191.
28. Sambrook, J., E. F. Fritsch, and T. Maniatis. 1989. Molecular cloning: a laboratory manual, 2nd ed., vol. 1, p. 5.8. Cold Spring Harbor Laboratory Press, New York, NY.
29. Selwood, A. I., P. T. Holland, S. A. Wood, K. F. Smith, and P. S. McNabb. 2007. Production of anatoxin-a and a novel biosynthetic precursor by the cyanobacterium Aphanizomenon issatschenkoi. Environ. Sci. Technol. 41: 506-510.
30. Sivonen, K., K. Himberg, R. Luukkainen, S. I. Niemelä, G. K. Poon, and G. A. Codd. 1989. Preliminary characterization of neurotoxic cyanobacteria blooms and strains from Finland. Toxic. Assess. 4:339-352.
31. Sivonen, K., and G. Jones. 1999. Cyanobacterial toxins, p. 41-111. In I. Chorus and J. Bartram (ed.), Toxic cyanobacteria in water: a guide line to public health significance, monitoring and management. E&FN Spon, London, United Kingdom.
32. 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.
33. Skulberg, O. M., W. W. Carmichael, R. A. Andersen, S. Matsunaga, R. E. Moore, and R. Skulberg. 1992. Investigations of a neurotoxic oscillatorialean strain (Cyanophyceae) and its toxin. Isolation and characterization of homoanatoxin-a. Environ. Toxicol. Chem. 11:321-329.
34. Stevens, D. K., and R. I. Krieger. 1991. Stability studies on the cyanobacterial nicotinic alkaloid anatoxin-a. Toxicon 29:167-179.
35. Tandeau de Marsac, N., and J. Houmard. 1988. Complementary chromatic adaptation: physiological conditions and action spectra. Methods Enzymol. 167:318-328.
36. 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.
37. Viaggiu, E., S. Melchiorre, F. Volpi, A. Di Corcia, R. Mancini, L. Garibaldi, G. Crichigno, and M. Bruno. 2004. Anatoxin-a toxin in the cyanobacterium Planktothrix rubescens from a fishing pond in northern Italy. Environ. Toxicol. 19:191-197.
38. Wood, S. A., J. P. Rasmussen, P. T. Holland, R. Campbell, and A. L. M. Crowe. 2007. First report of cyanotoxin anatoxin-a from Aphanizomenon issatschenkoi (cyanobacteria). J. Phycol. 43:356-365.
39. Wood, S. A., A. I. Selwood, A. Rueckert, P. T. Holland, J. R. Milne, K. F. Smith, B. Smits, L. F. Watts, and C. S. Cary. 2007. First report of homoanatoxin-a and associated dog neurotoxicosis in New Zealand. Toxicon 50:292-301.