1887

Abstract

The taxonomic coherence and phylogenetic relationships of 11 planktonic heterocystous cyanobacterial isolates were examined by investigating two areas of the rRNA operon, the 16S rRNA gene () and the internal transcribed spacer (ITS) located between the 16S rRNA and 23S rRNA genes. The sequences were determined for five strains, including representatives of -, -, sp. and two alkaliphilic planktonic members of the genera and , whose phylogenetic position was previously unknown. Comparison of the data with those previously published for individual groups of planktonic heterocystous cyanobacteria showed that, with the exception of members assigned to the genus , all the planktonic strains form a distinct subclade within the monophyletic clade of heterocystous cyanobacteria. Within this subclade five different phylogenetic clusters were distinguished. The phylogenetic groupings of and strains within three of these clusters were not always consistent with their generic or specific assignments based on classical morphological definitions, and the high degree of sequence similarity between strains of and suggests that they may be assignable to a single genus. Ribotyping and additional studies performed on PCR amplicons of the 16S rDNA or the ITS for the 11 planktonic heterocystous strains demonstrated that they all contain multiple operons and ITS regions of variable size. Finally, evidence is provided for intra-genomic sequence heterogeneity of the 16S rRNA genes within most of the individual isolates.

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2002-02-01
2019-09-15
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References

  1. Aubel, D., Renaud, F. N. & Freney, J. ( 1997; ). Genomic diversity of several Corynebacterium species identified by amplification of the 16S–23S gene spacer regions. Int J Syst Bacteriol 47, 767-772.[CrossRef]
    [Google Scholar]
  2. Barker, G. L. A., Hayes, P. K., O’Mahony, S. L., Vacharapiyasophon, P. & Walsby, A. E. ( 1999; ). A molecular and phenotypic analysis of Nodularia (cyanobacteria) from the Baltic Sea. J Phycol 35, 931-937.[CrossRef]
    [Google Scholar]
  3. Barker, G. L. A., Konopka, A., Handley, B. A. & Hayes, P. K. ( 2000; ). Genetic variation in Aphanizomenon (cyanobacteria) colonies from the Baltic Sea and North America. J Phycol 36, 947-950.[CrossRef]
    [Google Scholar]
  4. Beltran, E. C. & Neilan, B. A. ( 2000; ). Geographical segregation of the neurotoxin-producing cyanobacterium Anabaena circinalis. Appl Environ Microbiol 66, 4468-4474.[CrossRef]
    [Google Scholar]
  5. Bolch, C. J. S., Orr, T. P., Jones, G. J. & Blackburn, S. I. ( 1999; ). Genetic, morphological, and toxicological variation among globally distributed strains of Nodularia (Cyanobacteria). J Phycol 35, 339-355.[CrossRef]
    [Google Scholar]
  6. Booker, M. J. & Walsby, A. E. ( 1979; ). The relative form resistance of straight and helical blue-green algal filaments. Br Phycol J 14, 141-150.[CrossRef]
    [Google Scholar]
  7. Boyer, S. L., Flechtner, V. R. & Johansen, J. R. ( 2001; ). Is the 16S–23S internal transcribed spacer region a good tool for use in molecular systematics and population genetics? A case study in cyanobacteria. Mol Biol Evol 18, 1057-1069.[CrossRef]
    [Google Scholar]
  8. Carmichael, W. W. & Gorham, P. R. ( 1978; ). Anatoxins from clones of Anabaena flos-aquae isolated from lakes of Western Canada. Mitt Int Ver Limnol 21, 285-295.
    [Google Scholar]
  9. Carmichael, W. W. & Gorham, P. R. ( 1980; ). Freshwater cyanophyte toxins: types and their effects on the use of microalgal biomass. In Algal Biomass: Production and Use , pp. 437-448. Edited by G. Shelef & C. J. Soeder. Amsterdam:Elsevier.
  10. Cilia, V., Lafay, B. & Christen, R. ( 1996; ). Sequence heterogeneity among 16S rRNA sequences, and their effect on phylogenetic analyses at the species level. Mol Biol Evol 13, 451-461.[CrossRef]
    [Google Scholar]
  11. Clayton, R., Sutton, G., Hinkle, P. J., Bult, C. & Fields, C. ( 1995; ). Intraspecific variation in small-subunit rRNA sequences in GenBank: why single sequences may not adequately represent prokaryotic taxa. Int J Syst Bacteriol 45, 595-599.[CrossRef]
    [Google Scholar]
  12. Dennis, P. P., Ziesche, S. & Mylvaganam, S. ( 1998; ). Transcription analysis of two disparate rRNA operons in the halophilic archaeon Haloarcula marismortui. J Bacteriol 180, 4804-4813.
    [Google Scholar]
  13. Fergusson, K. M. & Saint, C. P. ( 2000; ). Molecular phylogeny of Anabaena circinalis and its identification in environmental samples by PCR. Appl Environ Microbiol 66, 4145-4148.[CrossRef]
    [Google Scholar]
  14. Florenzano, G., Sili, C., Pelosi, E. & Vincenzini, M. ( 1985; ). Cyanospira rippkae and Cyanospira capsulata (gen. nov. and spp. nov): new filamentous heterocystous cyanobacteria from Magadi lake (Kenya). Arch Microbiol 140, 301-306.[CrossRef]
    [Google Scholar]
  15. Giovannoni, S. J., Turner, S., Olsen, G. J., Barns, S., Lane, D. J. & Pace, N. R. ( 1988; ). Evolutionary relationships among cyanobacteria and green chloroplasts. J Bacteriol 170, 3584-3592.
    [Google Scholar]
  16. Gojobori, T., Ishii, K. & Nei, M. ( 1982; ). Estimation of average number of nucleotide substitutions when the rate of substitution varies with nucleotide. J Mol Evol 18, 414-423.[CrossRef]
    [Google Scholar]
  17. Hain, T., Ward-Rainey, N., Kroppenstedt, R. M., Stackebrandt, E. & Rainey, F. A. ( 1997; ). Discrimination of Streptomyces albidoflavus strains based on the size and number of 16S–23S rDNA intergenic spacers. Int J Syst Bacteriol 47, 202-206.[CrossRef]
    [Google Scholar]
  18. Horecká, M. & Komárek, J. ( 1979; ). Taxonomic position of three planktonic blue-green algae from the genera Aphanizomenon and Cylindrospermopsis. Preslia 51, 289-312.
    [Google Scholar]
  19. Iteman, I., Rippka, R., Tandeau de Marsac, N. & Herdman, M. ( 1999; ). Use of molecular tools for the study of genetic relationships of heterocystous cyanobacteria. In Marine Cyanobacteria (Bulletin de l’Institut Océanographique, Monaco, special issue 19) , pp. 13-20. Edited by L. Charpy & A. Larkum. Monaco:Institut Océanographique.
  20. Iteman, I., Rippka, R., Tandeau de Marsac, N. & Herdman, M. ( 2000; ). Conserved structural and regulatory domains within divergent 16S rRNA–23S rRNA spacer sequences of cyanobacteria. Microbiology 146, 1275-1286.
    [Google Scholar]
  21. Jeeji-Bai, N., Hegewald, E. & Soeder, C. J. ( 1977; ). Revision and taxonomic analysis of the genus Anabaenopsis. Arch Hydrobiol Suppl 51, 3-24.
    [Google Scholar]
  22. Jensen, M. A., Webster, J. A. & Straus, N. ( 1993; ). Effect of PCR conditions on the formation of the heteroduplex and single-stranded DNA products in the amplification of bacterial rDNA spacers regions. PCR Methods Appl 3, 186-194.[CrossRef]
    [Google Scholar]
  23. Kaneko, T., Sato, S., Kotani, H. & 21 other authors ( 1996; ). Sequence analysis of the genome of the unicellular cyanobacterium Synechocystis sp. strain PCC 6803. II. Sequence determination of the entire genome and assignment of potential protein-coding regions. DNA Res 3, 109–136.[CrossRef]
    [Google Scholar]
  24. Keswani, J. & Whitman, W. B. ( 2001; ). Relationship of 16S rRNA sequence similarity to DNA hybridization in prokaryotes. Int J Syst Evol Microbiol 51, 667-678.
    [Google Scholar]
  25. Lachance, M. A. ( 1981; ). Genetic relatedness of heterocystous cyanobacteria by deoxyribonucleic acid–deoxyribonucleic acid reassociation. Int J Syst Bacteriol 31, 139-147.[CrossRef]
    [Google Scholar]
  26. Lehtimäki, J., Lyra, C., Suomalainen, S., Sundman, P., Rouhiainen, L., Paulin, L., Salkinoja-Salonen, M. & Sivonen, K. ( 2000; ). Characterization of Nodularia strains, cyanobacteria from brackish waters, by genotypic and phenotypic methods. Int J Syst Evol Microbiol 50, 1043-1053.[CrossRef]
    [Google Scholar]
  27. Li, R., Carmichael, W. W., Liu, Y. & Watanabe, M. M. ( 2000; ). Taxonomic re-evaluation of Aphanizomenon flos-aquae NH-5 based on morphology and 16S rRNA gene sequences. Hydrobiologia 438, 99-105.[CrossRef]
    [Google Scholar]
  28. Liefting, L., Andersen, M., Beever, R., Gardner, R. & Forster, R. ( 1996; ). Sequence heterogeneity in the two 16S rRNA genes of Phormium yellow leaf phytoplasma. Appl Environ Microbiol 62, 3133-3139.
    [Google Scholar]
  29. Ligon, P. J. B., Meyer, K. G., Martin, J. A. & Curtis, S. E. ( 1991; ). Nucleotide sequence of a 16S rRNA gene from Anabaena sp. strain PCC 7120. Nucleic Acids Res 19, 4553.[CrossRef]
    [Google Scholar]
  30. Lu, W., Evans, H. E., McColl, M. & Saunders, V. A. ( 1997; ). Identification of cyanobacteria by polymorphisms of PCR-amplified rDNA spacer region. FEMS Microbiol Lett 153, 141-149.[CrossRef]
    [Google Scholar]
  31. Ludwig, W., Strunk, O., Klugbauer, S., Klugbauer, N., Weizenegger, M., Neumaier, J., Bachleitner, M. & Schleifer, K.-H. ( 1998; ). Bacterial phylogeny based on comparative sequence analysis. Electrophoresis 19, 554-568.[CrossRef]
    [Google Scholar]
  32. Lyra, C., Hantula, J., Vainio, E., Rapala, J., Rouhiainen, L. & Sivonen, K. ( 1997; ). Characterization of cyanobacteria by SDS-PAGE of whole-cell proteins and PCR/RFLP of the 16S rRNA gene. Arch Microbiol 168, 176-184.[CrossRef]
    [Google Scholar]
  33. Lyra, C., Suomalainen, S., Gugger, M., Vezie, C., Sundman, P., Paulin, L. & Sivonen, K. ( 2001; ). Molecular characterization of planktic cyanobacteria of Anabaena, Aphanizomenon, Microcystis and Planktothrix genera. Int J Syst Evol Microbiol 51, 513-526.
    [Google Scholar]
  34. Mahmood, N. A. & Carmichael, W. W. ( 1986; ). The pharmacology of anatoxin-a(s), a neurotoxin produced by the freshwater cyanobacterium Anabaena flos-aquae NRC 525-17. Toxicon 24, 425-434.[CrossRef]
    [Google Scholar]
  35. Martin, C., Sivonen, K., Matern, U., Dierstein, R. & Weckesser, J. ( 1990; ). Rapid purification of the peptide toxins microcystin-LR and nodularin. FEMS Microbiol Lett 68, 1-6.[CrossRef]
    [Google Scholar]
  36. Martinez-Murcia, A. J., Anton, A. I. & Rodriguez-Valera, F. ( 1999; ). Patterns of sequence variation in two regions of the 16S rRNA multigene family of Escherichia coli. Int J Syst Bacteriol 49, 601-610.[CrossRef]
    [Google Scholar]
  37. Miao, V. P. W., Rabenau, A. & Lee, A. ( 1997; ). Cultural and molecular characterization of photobionts of Peltigera membranacea. Lichenologist 29, 571-586.
    [Google Scholar]
  38. Moffitt, M. C., Blackburn, S. I. & Neilan, B. A. ( 2001; ). rRNA sequences reflect the ecophysiology and define the toxic cyanobacteria of the genus Nodularia. Int J Syst Evol Microbiol 51, 505-512.
    [Google Scholar]
  39. Mylvaganam, S. & Dennis, P. P. ( 1992; ). Sequence heterogeneity between the two genes encoding 16S rRNA from the halophilic archaebacterium Haloarcula marismortui. Genetics 130, 399-410.
    [Google Scholar]
  40. Neilan, B. A., Jacobs, D. & Goodman, A. E. ( 1995; ). Genetic diversity and phylogeny of toxic cyanobacteria determined by DNA polymorphisms within the phycocyanin locus. Appl Environ Microbiol 61, 3875-3883.
    [Google Scholar]
  41. Neilan, B. A., Stuart, J. L., Goodman, A. E., Cox, P. T. & Hawkins, P. R. ( 1997; ). Specific amplification and restriction polymorphisms of the cyanobacterial rRNA operon spacer region. Syst Appl Microbiol 20, 612-621.[CrossRef]
    [Google Scholar]
  42. Nichols, J. M., Foulds, I. J., Crouch, D. H. & Carr, N. G. ( 1982; ). The diversity of cyanobacterial genomes with respect to rRNA cistrons. J Gen Microbiol 128, 2739-2746.
    [Google Scholar]
  43. Nübel, U., Engelen, B., Felske, A., Snaidr, J., Wieshuber, A., Amann, R. I., Ludwig, W. & Backhaus, H. ( 1996; ). Sequence heterogeneities of genes encoding 16S rRNAs in Paenibacillus polymyxa detected by temperature gradient gel electrophoresis. J Bacteriol 178, 5636-5643.
    [Google Scholar]
  44. Olsen, G. J., Matsuda, H., Hagstrom, R. & Overbeek, R. ( 1994; ). fastDNAml: a tool for construction of phylogenetic trees of DNA sequences using maximum-likelihood. Comput Appl Biosci 10, 41-48.
    [Google Scholar]
  45. Rippka, R. & Herdman, M. (1992). Catalogue of Strains. Pasteur Culture Collection of Cyanobacterial Strains in Axenic Culture. Paris: Institut Pasteur.
  46. Rippka, R., Deruelles, J., Waterbury, J. B., Herdman, M. & Stanier, R. Y. ( 1979; ). Generic assignments, strain histories and properties of pure cultures of cyanobacteria. J Gen Microbiol 111, 1-61.[CrossRef]
    [Google Scholar]
  47. Rippka, R., Castenholz, R. W. & Herdman, M. (2001). Subsection IV. (Formerly Nostocales Castenholz 1989b sensu Rippka, Deruelles, Waterbury, Herdman and Stanier 1979). In Bergey’s Manual of Systematic Bacteriology, 2nd edn, vol. 1, The Archaea and the Deeply Branching and Phototrophic Bacteria, pp. 562–589. Edited by D. R. Boone, R. W. Castenholz & G. M. Garrity. New York: Springler-Verlag.
  48. Rosselló-Mora, R. & Amann, R. ( 2001; ). The species concept for prokaryotes. FEMS Microbiol Rev 25, 39-67.[CrossRef]
    [Google Scholar]
  49. Saker, M. L. & Neilan, B. A. ( 2001; ). Varied diazotrophies, morphologies, and toxicities of genetically similar isolates of Cylindrospermopsis raciborskii (Nostocales, Cyanophyceae) from Northern Australia. Appl Environ Microbiol 67, 1839-1845.[CrossRef]
    [Google Scholar]
  50. Sambrook, J., Fritsch, E. F. & Maniatis, T. (1989). Molecular Cloning: a Laboratory Manual, 2nd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
  51. Schlösser, U. G. ( 1994; ). Sammlung von Algenkulturen at the University of Göttingen. Catalogue of strains. Bot Acta 107, 111-186.[CrossRef]
    [Google Scholar]
  52. Seenayya, G. & Subba-Raju, N. ( 1972; ). On the ecology and systematic position of the alga known as Anabaenopsis raciborskii (Wolosz.) Elenk. and a critical evaluation of the forms described under the genus Anabaenopsis. In Taxonomy and Biology of Blue-green Algae , pp. 52-57. Edited by T. V. Desikachary. Madras:University of Madras.
  53. Sivonen, K. & Jones, G. ( 1999; ). Cyanobacterial toxins. In Toxic Cyanobacteria in Water. A Guide to Their Public Health Consequences, Monitoring and Management , pp. 41-111. Edited by I. Chorus & J. Bartram. London:E. & F. N. Spon on behalf of the WHO.
  54. Turner, S. ( 1997; ). Molecular systematics of oxygenic photosynthetic bacteria. Plant Syst Evol (Suppl) 11, 13-52.
    [Google Scholar]
  55. Ueda, K., Seki, T., Kudo, T., Yoshida, T. & Kataoka, M. ( 1999; ). Two distinct mechanisms cause heterogeneity of 16S rRNA. J Bacteriol 181, 78-82.
    [Google Scholar]
  56. Van de Peer, Y. & De Wachter, R. ( 1994; ). treecon for Windows: a software package for the construction and drawing of evolutionary trees for the Microsoft Windows environment. Comput Appl Biosci 10, 569-570.
    [Google Scholar]
  57. Walsby, A. E. ( 1981; ). Cyanobacteria: planktonic gas-vacuolate forms. In The Prokaryotes , pp. 224-235. Edited by M. P. Starr, H. Stolp, H. G. Trüper, A. Balows & H. G. Schlegel. Berlin, Heidelberg, New York:Springer-Verlag.
  58. Wang, Y., Zhang, Z. & Ramanan, N. ( 1997; ). The actinomycete Thermobispora bispora contains two distinct types of transcriptionally active 16S rRNA genes. J Bacteriol 179, 3270-3276.
    [Google Scholar]
  59. Wayne, L. G., Brenner, D. J., Colwell, R. R. & 9 other authors ( 1987; ). Report of the Ad Hoc Committee on reconciliation of approaches to Bacterial Systematics. Int J Syst Bacteriol 37, 463–464.[CrossRef]
    [Google Scholar]
  60. West, N. J. & Adams, D. G. ( 1997; ). Phenotypic and genotypic comparison of symbiotic and free-living cyanobacteria from a single field site. Appl Environ Microbiol 63, 4479-4484.
    [Google Scholar]
  61. Wilmotte, A. & Herdman, M. (2001). Phylogenetic relationships among the cyanobacteria based on 16S rRNA sequences. Bergey’s Manual of Systematic Bacteriology, 2nd edn, vol. 1, The Archaea and the Deeply Branching and Phototrophic Bacteria, pp. 487–493. Edited by D. R. Boone, R. W. Castenholz & G. M. Garrity. New York: Springler-Verlag.
  62. Wilmotte, A., Van der Auwera, G. & De Wachter, R. ( 1993; ). Structure of the 16S rRNA of the thermophilic cyanobacterium Chlorogloeopsis HTF (‘Mastigocladus laminosus HTF’) strain PCC 7518, and phylogenetic analysis. FEBS Lett 317, 96-100.[CrossRef]
    [Google Scholar]
  63. Wilson, K. M., Schembri, M. A., Baker, P. D. & Saint, C. P. ( 2000; ). Molecular characterization of the toxic cyanobacterium Cylindrospermopsis raciborskii and design of a species-specific PCR. Appl Env Microbiol 66, 332-338.[CrossRef]
    [Google Scholar]
  64. Yap, W. H., Zhang, Z. & Wang, Y. ( 1999; ). Distinct types of rRNA operons exist in the genome of the Actinomycete Thermomonospora chromogena and evidence for horizontal transfer of an entire rRNA operon. J Bacteriol 181, 5201-5209.
    [Google Scholar]
  65. Zevenboom, W., Van Der Does, J., Bruning, K. & Mur, L. R. ( 1981; ). A non-heterocystous mutant of Aphanizomenon flos-aquae, selected by competition in light-limited continuous culture. FEMS Microbiol Lett 10, 11-16.[CrossRef]
    [Google Scholar]
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