Advertisement

Hydrobiologia

, Volume 468, Issue 1–3, pp 135–145 | Cite as

A molecular test of cyanobacterial phylogeny: inferences from constraint analyses

  • M. K. Litvaitis
Article

Abstract

Parsimony and neighbor-joining analyses of 16S rDNA nucleotide sequences of 68 species and strains of cyanobacteria and prochlorophytes supported a monophyletic Nostocales, a monophyletic Stigonematales, three independent lineages of prochlorophytes within the cyanobacteria, and a paraphyletic Chroococcales (p<0.0001) and Oscillatoriales (p = 0.0147). Within the Oscillatoriales, the genus Oscillatoria formed an unnatural taxon (p<0.0001) and needs major revisions. Using constraint analysis, the genus Microcystis was found to be monophyletic and the paraphyletic positions of Microcystis elabens and M. holsatica are probably due to long-branch attraction. Further, a separation of Chroococcales based on varying levels of polyunsaturated fatty acids is more consistent with nucleotide-based phylogenies than with existing morphological groupings. It is proposed that Chroococcales be redefined to exclude the genus Microcystis, and that a new order be erected for Microcystis. Finally, it is more parsimonious to assume a common cyanobacterial/prochlorophyte ancestor, than to evoke de novo synthesis of chlb in each prochlorophyte lineage plus in the lineage leading to green chloroplasts. This common ancestor is proposed to have contained both chlorophyll a and b plus phycobilins. Subsequent multiple losses of chlb in cyanobacteria and the loss of chla and phycobilins in prochlorophytes, led to the currently observed pigment distribution. It is therefore, recommended that Prochlorales be reclassified as cyanobacteria.

16S rDNA Microcystis distance- and parsimony methods 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Anagnostidis, K. & J. Komárek, 1985. Modern approach to the classification system of cyanophytes. 1. Introduction. Arch. Hydrobiol., Suppl. 71, Algol. Studies 38/39: 291–302.Google Scholar
  2. Anagnostidis, K. & J. Komárek, 1988. Modern approach to the classification system of cyanophytes. 3. Oscillatoriales. Arch. Hydrobiol., Suppl. 80, Algol. Studies 50/53: 327–472.Google Scholar
  3. Anagnostidis, K. & J. Komárek, 1990. Modern approach to the classification system of cyanophytes. 5. Stigonematales. Arch. Hydrobiol., Suppl. 86, Algol. Studies 59: 1–73.Google Scholar
  4. Burger‐Wiersma, T., M. Veenhuis, H. J. Korthals, C. C. M. Van de Wiel & L. R. Mur, 1986. A new prokaryote containing Chlsa and b. Nature 320: 262–264.Google Scholar
  5. Castenholz, R. W. & J. B. Waterbury, 1989. Oxygenic photosynthetic bacteria sect 19., Group I. Cyanobacteria. In Staley, J. T., M. P. Bryant, N. Pfennig & J. G. Holt (eds), Bergey's Manual of Systematic Bacteriology. Vol 3. Williams and Wilkins Co, Baltimore: 1710–1728.Google Scholar
  6. Chisholm, S. W., R. J. Olson, E. R. Zettler, R. Goericke, J. B. Waterbury & N. A. Welschmeyer, 1988. A novel free-living prochlorophyte abundant in the oceanic euphotic zone. Nature 334: 340–343.Google Scholar
  7. Delwiche, C. F. & J. D. Palmer, 1996. Rampant horizontal transfer and duplication of Rubisco genes in eubacteria and plastids. Mol. Biol. Evol. 13: 873–882.Google Scholar
  8. Desikachary, T., 1973. Status of classical taxonomy. In Carr, N. G. & B. A. Whitton (eds), The Biology of Blue-Green Algae. University of California Press, Berkeley: 473–486.Google Scholar
  9. Drouet, F., 1981. Summary of the classification of blue-green algae. Beihefte Nova Hedwigia 66: 135–209.Google Scholar
  10. Felsenstein, J., 1978. Cases in which parsimony or compatibility methods will be positively misleading. Syst. Zool. 40: 366–375.Google Scholar
  11. Florenzano, G., W. Balloni & R. Materassi, 1986. Nomenclature of Prochloron didemni (Lewin, 1977) sp. n., nom. rev., Prochloron (Lewin, 1976) gen. n., nom. rev., Prochloraceae fam. n., Prochlorales ord. n., nom. rev. in the class Photobacteria Gibbons and Murray 1978. Internat. J. Syst. Bacteriol. 36: 351–353.Google Scholar
  12. Garcia‐Pichel, F., U. Nubel & G. Muyzer, 1998. The phylogeny of unicellular, extremely halotolerant cyanobacteria. Arch. Microbiol. 169: 469–482.Google Scholar
  13. Geitler, L., 1925. Synoptische Darstellung der Cyanophyceen in morphologischer und systematischer Hinsicht. Beih. Bot. Centralbl. 2: 163–324.Google Scholar
  14. Geitler, L., 1932. Cyanophyceae. In Kolkwitz, R. (ed.), Rabenhorst's Kryptogamenflora von Deutschland, österreich und der Schweiz. Vol XIV. Akadem. Verlagsgesellsch., Leipzig. Reprinted 1971, Johnson, New York: 1–1196.Google Scholar
  15. Holton, R. W., H. H. Blecker & T. S. Stevens, 1968. Fatty acids in the blue-green algae: possible relation to phylogenetic position. Science 160: 545–547.Google Scholar
  16. Honda, D., A. Yokota & J. Sugiyama, 1999. Detection of seven major evolutionary lineages in cyanobacteria based on 16S rRNA gene sequence analysis with new sequences of five marine Synechococcus strains. J. Mol. Evol. 48: 723–739.Google Scholar
  17. Higgins, D. G., A. J. Bleasby & R. Fuchs, 1992. CLUSTAL V: improved software for multiple sequence alignment. Comp. Appl. Biosci. 8: 189–191.Google Scholar
  18. Johns, R. B., P. D. Nichols, F. T. Gillian, G. J. Perry & J. K. Volkman, 1981. Lipid composition of the symbiotic prochlorophyte in relation to the host. Comp. Biochem. Physiol. 69B: 843–849.Google Scholar
  19. Kenyon, C. N., 1972. Fatty acid composition of unicellular strains of blue-green algae. J. Bacteriol. 109: 827–834.Google Scholar
  20. Kenyon, C. N., R. Rippka & R. Y. Stanier, 1972. Fatty acid composition and physiological properties of some filamentous blue-green algae. Arch. Microbiol. 83: 216–236.Google Scholar
  21. Komárek, J. & K. Anagnostidis, 1986. Modern approach to the classification system of cyanophytes. 2. Chroococcales. Arch. Hydrobiol., Suppl. 73, Algol. Studies 43: 157–226.Google Scholar
  22. Komárek, J. & K. Anagnostidis, 1989. Modern approach to the classification system of cyanophytes. 4. Nostocales. Arch. Hydrobiol., Suppl. 82, Algol. Studies 56: 247–345.Google Scholar
  23. Kondo, R., M. Komura, S. Hiroishi & Y. Hata, 1998. Detection and 16S rDNA sequence analysis of a bloom-forming cyanobacterial genus Microcystis. Fish. Sci. 64: 840–841.Google Scholar
  24. Lachance, M.-A., 1981. Genetic relatedness of heterocystous cyanobacteria by deoxyribonucleic acid-deoxyribonucleic acid reassociation. Int. J. Syst. Bact. 31: 139–147.Google Scholar
  25. Larson, A., 1994. The comparison of morphological and molecular data in phylogenetic systematics. In Schierwater, B., B. Streit, G. B. Wagner & R. DeSalle (eds), Molecular Ecology and Evolution: Approaches and Applications. Birkhäuser Verlag, Basel: 371–390.Google Scholar
  26. Lewin, R. A., 1976. Prochlorophyta as a proposed new division of algae. Nature 261: 697–698.Google Scholar
  27. Lewin, R. A., 1977. Prochloron, type genus of the Prochlorophyta. Phycologia 16: 217.Google Scholar
  28. Lewin, R. A., 1981. Prochloron and the theory of symbiogenesis. Ann. New York Acad. Sci. 361: 325–329.Google Scholar
  29. Lewin, R. A., 1984. Prochloron — a status report. Phycologia 23: 203–204.Google Scholar
  30. Lockhart, P. J., M. A. Steel, M. D. Hendy & D. Penny, 1994. Recovering evolutionary trees under a more realistic model of sequence evolution. Mol. Biol. Evol. 11: 605–621.Google Scholar
  31. Matthijs, H. C. P., G. W. M. Van der Staay & L. R. Mur, 1994. Prochlorophytes: The 'other’ cyanobacteria? In Bryant, D. A. (ed.), The Molecular Biology of Cyanobacteria. Kluwer Academic Publishers, Dordrecht, The Netherlands: 49–64.Google Scholar
  32. Mazel, D., J. Houmard, A. M. Castets & N. Tabdeau de Marsac, 1990. Highly repetitive DNA sequences in cyanobacterial genomes. J. Bacteriol. 172: 2755–2761.Google Scholar
  33. Morden, C. W. & S. S. Golden, 1989. psbA genes indicate common ancestry of prochlorophytes and chloroplasts. Nature 337: 383–385.Google Scholar
  34. Miller, K. R. & J. S. Jacob, 1989. On Prochlorothrix. Nature 338: 303–304.Google Scholar
  35. Neilan, B., D. Jacobs, T. Del Dot, L. Blackall, P. R. Hawkins, P. T. Cox & A. E. Goodman, 1997. rRNA sequences and evolutionary relationships among toxic and non-toxic cyanobacteria of the genus Microcystis. Internat. J. Syst. Bacteriol. 47: 693–697.Google Scholar
  36. Nelissen, B., R. De Baere, A. Wilmotte & R. De Wachter, 1996. Phylogenetic relationships of nonaxenic filamentous cyanobacterial strains based on 16S rDNA sequence analysis. J. Mol. Evol. 42: 194–200.Google Scholar
  37. Palenik, B. & R. Haselkorn, 1992. Multiple evolutionary origins of prochlorophytes, the chlorophyll b-containing prokaryotes. Nature 355: 265–267.Google Scholar
  38. Pearson, J. E. & J.M. Kingsbury, 1966. Culturally induced variation in four morphologically diverse blue-green algae. Am. J. Bot. 53: 192–200.Google Scholar
  39. Rippka, R. & M. Herdman, 1992. Pasteur Culture Collection of Cyanobacteria. Catalogue and Taxonomic Handbook. Vol I: Catalogue of Strains. Institute Pasteur, Paris: 103 pp.Google Scholar
  40. Rippka, R., J. Deruelles, J. B. Waterbury, M. Herdman & R. Y. Stanier, 1979. Generic assignments, strain histories and properties of pure cultures of cyanobacteria. J. Gen. Microbiol. 111: 1–61.Google Scholar
  41. Rudi, K., O. M. Skulberg & K. S. Jakobsen, 1998. Evolution of cyanobacteria by exchange of genetic material among phyletically related strains. J. Bacteriol. 180: 3453–3461.Google Scholar
  42. Saitou, N. & M. Nei, 1987. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 4: 406–425.Google Scholar
  43. Stam, W. T., 1980. Relationships between a number of filamentous blue-green algal strains Cyanophyceae. revealed by DNA-DNA hybridization. Arch. Hydrobiol., Suppl. 56, Algol. Studies 25: 351–374.Google Scholar
  44. Stam, W. T. & G. Venema, 1975. The use of DNA-DNA hybridization for determination of the relationship between some blue-green algae Cyanophyceae. Acta Bot. Neerland. 26: 327–342.Google Scholar
  45. Stanier, R. Y., W. R. Sistrom, T. A. Hansen, B. A. Whitton, R. W. Castenholz, N. Pfennig, V. N. Gorlenko, E. N. Kondratieva, K. E. Eimhjellen, R. Whittenbury, R. L. Gherna & H. G. Trüper, 1978. Proposal to place the nomenclature of the cyanobacteria blue-green algae under the rules of the International Code of Nomenclature of Bacteria. International J. Syst. Bacteriol. 28: 335–336.Google Scholar
  46. Swofford, D., 1999. PAUP*: Phylogenetic Analysis Using Parsimony (and other methods), vers. 4.0, Sinauer Associates, Sunderland, MA.Google Scholar
  47. Tomitani, A., K. Okada, H. Miyashita, H. C. Matthijs, T. Ohno & A. Tanaka, 1999. Chlorophyll b and phycobilins in the common ancestor of cyanobacteria and chloroplasts. Nature 400: 159–162.Google Scholar
  48. Turner, S., T. Burger-Wiersma, S. J. Giovannoni, L. R. Murt & N. R. Pace, 1989. The relationship of a prochlorophyte Prochlorothrix hollandica to green chloroplasts. Nature 337: 380–382.Google Scholar
  49. Urbach, E., D. L. Robertson & S. W. Chisholm, 1992. Multiple evolutionary origins of prochlorophytes within the cyanobacterial radiation. Nature 355: 267–270.Google Scholar
  50. Urbach, E., D. J. Scanlan, D. L. Distel, J. B. Waterbury & S. W. Chisholm, 1998. Rapid diversification of marine phytoplankton with dissimilar light-harvesting structures inferred from sequences of Prochlorococcus and Synechococcus (Cyanobacteria). J. Mol. Evol. 46: 188–201.Google Scholar
  51. Ward, D. M., M. M. Bateson, R. Weller & A. L. Ruff‐Roberts, 1992. Ribosomal RNA analysis of microorganisms as they occur in nature. Adv. Microbiol. Ecol. 12: 219–286.Google Scholar
  52. Waterbury, J. B. & R. Rippka, 1989. Oxygenic photosynthetic bacteria sect 19., Subsection I. Order Chroococcales. In Staley, J. T., M. P. Bryant, N. Pfennig & J. G. Holt (eds), Bergey's Manual of Systematic Bacteriology. Vol 3. Williams and Wilkins Co, Baltimore: 1729–1746.Google Scholar
  53. Wilmotte, A., 1994. Molecular evolution and taxonomy of cyanobacteria. In Bryant, D. A. (ed.), The Molecular Biology of Cyanobacteria. Kluwer Academic Publishers, Dordrecht, The Netherlands: 1–25.Google Scholar

Copyright information

© Kluwer Academic Publishers 2002

Authors and Affiliations

  • M. K. Litvaitis
    • 1
  1. 1.Department of Zoology and Center for Marine BiologyUniversity of New HampshireDurhamU.S.A.

Personalised recommendations