Phylogenetic evaluation of cyanobacteria preserved as historic herbarium exsiccata Free

Abstract

Dried herbarium specimens of cyanobacteria (exsiccata) deposited over 100 years ago were analysed and characterized using combined morphological and molecular approaches. Six representative coccoid and filamentous cyanobacteria from two historic collections and a 15-year-old air-dried environmental sample were studied. Morphological features observed by light and electron microscopy were correlated with the results of 16S rRNA gene sequencing. Historic identifications achieved by means of classical morphology could thus be confirmed by extracted, amplified and sequenced 16S rRNA gene fragments. The results of this study open the possibility of providing genotypic characterizations to botanical type specimens, thus reconciling the botanical and bacteriological approaches to the taxonomic treatment of these micro-organisms.

Loading

Article metrics loading...

/content/journal/ijsem/10.1099/ijs.0.64417-0
2006-10-01
2024-03-29
Loading full text...

Full text loading...

/deliver/fulltext/ijsem/56/10/2253.html?itemId=/content/journal/ijsem/10.1099/ijs.0.64417-0&mimeType=html&fmt=ahah

References

  1. Amann R. I., Ludwig W., Schleifer K.-H. 1995; Phylogenetic identification and in situ detection of individual microbial cells without cultivation. Microbiol Rev 59:143–169
    [Google Scholar]
  2. Bornet E., Flahault C. 1886; Révision des Nostocacées filamenteuses hétérocystées contenues dans les principaux herbiers de France. Ann Sci Nat Bot Paris Ser 37:323–381 (in French
    [Google Scholar]
  3. Castenholz R. W. 2001; General characteristics of the cyanobacteria. In Bergey's Manual of Systematic Bacteriology , 2nd edn. vol 1 pp  474–487 Edited by Boone D. R., Castenholz R. W. New York: Springer;
    [Google Scholar]
  4. Codd G. A., Bell S. G., Kaya K., Ward C. J., Beattie K. A., Metcalf J. S. 1999; Cyanobacterial toxins, exposure routes and human health. Eur J Phycol 34:405–415 [CrossRef]
    [Google Scholar]
  5. Cohan F. M. 2002; What are bacterial species?. Ann Rev Microbiol 56:457–487 [CrossRef]
    [Google Scholar]
  6. Cohn F. 1875; Untersuchungen über Bakterien. Beiträge Biol Planzen 1:127–222 (in German
    [Google Scholar]
  7. Doers M. P., Parker D. L. 1988; Properties of Microcystis aeruginosa and M. flos-aquae (Cyanophyta) in culture: taxonomic implications. J Phycol 24:502–508
    [Google Scholar]
  8. Dor I., Hornoff M. 1985; Salinity-temperature relations and morphotypes of a mixed population of coccoid cyanobacteria from a hot hypersaline pond in Israel. Mar Ecol 6:13–25 [CrossRef]
    [Google Scholar]
  9. Elenkin A. A. 1938 Sinezelenye vodorosli SSSR Monographia algarum cyanophycearum aquidulcium et terrestrium in finibus URSS inventarum . Pars spec 1, 2, Akad Moscow-Leningrad: Nauk SSSR;
    [Google Scholar]
  10. Garcia-Pichel F., Prufert-Bebout L., Muyzer G. 1996; Phenotypic and phylogenetic analyses show Microcoleus chthonoplastes to be a cosmopolitan cyanobacterium. Appl Environ Microbiol 62:3284–3291
    [Google Scholar]
  11. Garcia-Pichel F., Nübel U., Muyzer G. 1998; The phylogeny of unicellular, extremely halotolerant cyanobacteria. Arch Microbiol 169:469–482 [CrossRef]
    [Google Scholar]
  12. Geitler L. 1932; Cyanophyceae. In DrL. Rabenhorst's Kryptogamen-Flora von Deutschland Österreich und der Schweiz vol. XIV: Leipzig: Akademischer Verlag; (1985 reprint: KönigsteIn Koeltz Scientific Books;
    [Google Scholar]
  13. Gevers D., Cohan F. M., Lawrence J. G. 8 other authors 2005; Re-evaluating prokaryotic species. Nat Rev Microbiol 3:733–739 [CrossRef]
    [Google Scholar]
  14. Giovannoni S. J., Turner S., Olsen G. J., Barns J., Lane D. J., Pace N. R. 1988; Evolutionary relationships among cyanobacteria and green chloroplasts. J Bacteriol 170:3584–3592
    [Google Scholar]
  15. Giovannoni S. J., Britschgi T. B., Moyer C. L., Field K. G. 1990; Genetic diversity in Sargasso Sea bacterioplankton. Nature 345:60–63 [CrossRef]
    [Google Scholar]
  16. Golubic S. 1967; Zwei wichtige Merkmale zur Abgrenzung der Blaualgengattungen (Two important criteria for delimitation of cyanophyte genera). Schweiz Z Hydrol 29:175–184 (in German
    [Google Scholar]
  17. Golubic S., Marcenko E. 1965; Ueber Konvergenzerscheinungen bei Standortsformen der Blaualgen unter extremen Lebensbedingungen (Ecologically induced convergent morphologies in blue-green algae of extreme environments). Schweiz Z Hydrol 27:207–217 (in German
    [Google Scholar]
  18. Gomont M. 1892a; Monographie des Oscillariées. Ann Sci Nat Bot Paris 15:263–368
    [Google Scholar]
  19. Gomont M. 1892b; Monographie des Oscillariées. Ann Sci Nat Bot Paris 16:91–264
    [Google Scholar]
  20. Gorham P. R. 1964; Toxic algae. In Algae and Man pp  307–336 Edited by Jackson D. F. New York: Plenum Publishing Corp;
    [Google Scholar]
  21. Hoffmann L. 2005; Nomenclature of Cyanophyta/Cyanobacteria: roundtable on the unification of the nomenclature under the Botanical and the Bacteriological Codes. Arch Hydrobiol Suppl 159:13–29
    [Google Scholar]
  22. Honda D., Yokota A., Sugiyama J. 1999; Detection of seven major evolutionary lineages in cyanobacteria based on the 16S rRNA gene sequence analysis with new sequences of five marine Synechococcus strains. J Mol Evol 48:723–739 [CrossRef]
    [Google Scholar]
  23. Hugenholtz P., Goebel B. M., Pace N. R. 1998; Impact of culture-independent studies on the emerging phylogenetic view of bacterial diversity. J Bacteriol 180:4765–4774
    [Google Scholar]
  24. Janse I., Meima M. W., Kardinaal E. A., Zwart G. 2003; High-resolution differentiation of Cyanobacteria by using rRNA-internal transcribed spacer denaturing gradient gel electrophoresis. Appl Environ Microbiol 69:6634–6643 [CrossRef]
    [Google Scholar]
  25. Karsten U. 2002; Effects of salinity and ultraviolet radiation on the concentration of mycosporine-like amino acids in various isolates of the benthic cyanobacterium Microcoleus chthonoplastes . Phycological Res 50:129–134 [CrossRef]
    [Google Scholar]
  26. Komarek J., Anagnostidis K. 1999; Cyanoprokaryota, 1. Teil: Chroococcales. In Süsswasserflora von Mitteleuropa Band 19/1 pp  1–548 Edited by Ettl H., Gärtner G., Heynig H., Mollenhauer D. Jena: Gustav Fischer Verlag (in German);
    [Google Scholar]
  27. Komarek J., Anagnostidis K. 2005; Cyanoprokaryota. 2. Teil Oscillatoriales. In Süsswasserflora von Mitteleuropa Band 19/2 pp  1–757 Edited by Büdel B., Gärtner G., Krienitz L., Schagerl M. München: Elsevier Spectrum Akademischer Verlag (in German);
    [Google Scholar]
  28. Kossinskaya E. K. 1949; Opredelitel' Morskikh Sineselenykh Vodorosley [ Determination Key of Marine Blue-Green Algae ]. pp. 1–278 Akad. Moscow-Leningrad: Nauk USSR (in Russian)
  29. Lapage S. P., Sneath P. H. A., Lessel E. F., Skerman V. B. D., Seeliger H. P. R., Clark W. A. (editors) 1992 International Code of Nomenclature of Bacteria (1990 Revision) . Bacteriological Code Washington, DC: American Society for Microbiology;
    [Google Scholar]
  30. 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]
  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., 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]
  33. Lyra C., Laamanen M., Lehtimäki J. M., Surakka A., Sivonen K. 2005; Benthic cyanobacteria of the genus Nodularia are non-toxic, without gas vacuoles, able to glide and genetically more diverse than planktonic Nodularia . Int J Syst Evol Microbiol 55:555–568 [CrossRef]
    [Google Scholar]
  34. Mazur H., Pliński M. 2003; Nodularia spumigena blooms and the occurrence of hepatotoxin in the Gulf of Gdańsk. Oceanologia 45:305–316
    [Google Scholar]
  35. 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]
  36. Nadeau T. L., Milbrandt E. C., Castenholz R. W. 2001; Evolutionary relationships of cultivated Antarctic oscillatorians (cyanobacteria). J Phycol 37:650–654 [CrossRef]
    [Google Scholar]
  37. Nübel U., Garcia-Pichel F., Muyzer G. 1997; PCR primers to amplify 16S rRNA genes from Cyanobacteria. Appl Environ Microbiol 63:3327–3332
    [Google Scholar]
  38. Oren A. 2004; A proposal for further integration of the cyanobacteria under the Bacteriological Code. Int J Syst Evol Microbiol 54:1895–1902 [CrossRef]
    [Google Scholar]
  39. Oren A., Tindall B. J. 2005; Nomenclature of the cyanophyta/cyanobacteria/cyanoprokaryotes under the International Code of Nomenclature of Prokaryotes. Arch Hydrobiol Suppl 159:39–52
    [Google Scholar]
  40. Otsuka S., Suda S., Shibata S., Oyaizu H., Matsumoto S., Watanabe M. M. 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 [CrossRef]
    [Google Scholar]
  41. Palinska K. A., Liesack W., Rhiel E., Krumbein W. E. 1996; Phenotype variability of identical genotypes: the need for a combined approach in cyanobacterial taxonomy demonstrated on Merismopedia -like isolates. Arch Microbiol 166:224–233 [CrossRef]
    [Google Scholar]
  42. Paul V. J., Thacker R. W., Banks K., Golubic S. 2005; Benthic cyanobacterial bloom impact the reefs of South Florida (Broward County USA). Coral Reefs 24:693–697 [CrossRef]
    [Google Scholar]
  43. Rajaniemi P., Hrouzek P., Kastovska K., Willame R., Rantala A., Hoffmann L., Komarek J., Sivonen K. 2005; Phylogenetic and morphological evaluation of the genera Anabaena, Aphanizomenon, Trichormus and Nostoc (Nostocales, Cyanobacteria). Int J Syst Evol Microbiol 55:11–26 [CrossRef]
    [Google Scholar]
  44. Rippka R., Herdman M. 1992; Part 4: Strain List. In Pasteur Culture Collection of Cyanobacteria Catalogue & Taxonomic Handbook , vol. I: Catalogue of Strains (1992/1993) pp  12–59 Edited by Rippka R., Herdman M. Paris: Institut Pasteur;
    [Google Scholar]
  45. 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]
  46. Rossello-Mora R., Amann R. 2001; The species concept for prokaryotes. FEMS Microbiol Rev 25:39–67 [CrossRef]
    [Google Scholar]
  47. Stanier R. Y. 1977; Position of Cyanobacteria in the world of phototrophs. Carlsberg Res Comm 42:77–98 [CrossRef]
    [Google Scholar]
  48. Stanier R. Y., Cohen-Bazire G. 1977; Phototrophic prokaryotes: the cyanobacteria. Annu Rev Microbiol 31:225–274 [CrossRef]
    [Google Scholar]
  49. Stanier R. Y., Sistrom W. R., Hansen T. A. 9 other authors 1978; Proposal to place the nomenclature of the cyanobacteria (blue-green algae) under the rules of the International Code of Nomenclature of Bacteria. Int J Syst Bacteriol 28:335–336 [CrossRef]
    [Google Scholar]
  50. Surosz W., Palinska K. A. 2004; Effects of heavy metal stress on cyanobacterium Anabaena flos-aquae . Arch Environ Contam Toxicol 48:40–48 [CrossRef]
    [Google Scholar]
  51. Turner S. 1997; Molecular systematics of oxygenic photosynthetic bacteria. Plant Syst Evol Suppl 11:13–52
    [Google Scholar]
  52. Utkilen H., Skulberg R., Underdal B., Gjølme N., Skulberg R., Kotai J. 1996; The rise and fall of a toxigenic population of Microcystis aeruginosa (cyanophyceae/cyanobacteria) - a decade of observations in Lake Akersvatnet, Norway. Phycologia 35:189–197 [CrossRef]
    [Google Scholar]
  53. 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]
  54. Ward D. M., Ferris M. J., Nold S. C., Bateson M. M., Kopkczynski E. D., Ruff-Roberts A. L. 1994; Species diversity in hot spring microbial mats as revealed by both molecular and enrichment culture approach - relationship between biodiversity and community structure. In Microbial Mats, Structure, Development and Environmental Significance (NATO ASI Series G 35) pp  33–44 Edited by Stal L. J., Caumette P. Heidelberg: Springer;
    [Google Scholar]
  55. Ward D. M., Santegoeds C. M., Nold S. C., Ramsing N. B., Ferris M. J., Bateson M. M. 1997; Biodiversity within hot spring microbial mat communities: molecular monitoring of enrichment cultures. Antonie van Leeuwenhoek 71:143–150 [CrossRef]
    [Google Scholar]
  56. Waterbury J. B., Rippka R. 1989; Subsection I. Order Chroococcales Wettstein 1924, emend. Rippka et al. , 1979. In Bergey's Manual of Systematic Bacteriology vol. 3 pp  1728–1746 Edited by Staley J. T., Bryant M. P., Pfennig N., Holt J. G. Baltimore: Williams & Wilkins;
    [Google Scholar]
  57. Waterbury J. B., Stanier R. Y. 1977; Two unicellular cyanobacteria which reproduce by budding. Arch Microbiol 115:249–257 [CrossRef]
    [Google Scholar]
  58. Whitton B. A., Potts M. 2000; Introduction to the cyanobacteria. In The Ecology of Cyanobacteria pp  1–11 Edited by Whitton B. A., Potts M. Dordrecht: Kluwer Academic;
    [Google Scholar]
  59. Wilmotte A. 1994; Molecular evolution and taxonomy of the Cyanobacteria. In The Molecular Biology of Cyanobacteria pp  1–25 Edited by Bryant D. A. Dordrecht: Kluwer Academic Publishers;
    [Google Scholar]
  60. Wilmotte A., Herdman M. 2001; Phylogenetic relationships among the Cyanobacteria based on 16S rRNA sequences. In Bergey's Manual of Systematic Bacteriology , 2nd edn. vol 1 pp  487–493 Edited by Boone D. R., Castenholz R. W. New York: Springer;
    [Google Scholar]
  61. Woese C. R. 1987; Bacterial evolution. Microbiol Rev 51:221–271
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/ijsem/10.1099/ijs.0.64417-0
Loading
/content/journal/ijsem/10.1099/ijs.0.64417-0
Loading

Data & Media loading...

Most cited Most Cited RSS feed