Multiple evolutionary origins of prochlorophytes within the cyanobacterial radiation (original) (raw)

Nature volume 355, pages 267–270 (1992)Cite this article

Abstract

THE taxonomic group Prochlorales (Lewin 1977) Burger-Wiersma, Stal and Mur 1989 was established to accommodate a set of prokaryotic oxygenic phototrophs which, like plant, green algal and euglenoid chloroplasts, contain chlorophyll b instead of phycobiliproteins. Prochlorophytes were originally proposed (with concomitant scepticism1–3) to be a monophyletic group sharing a common ancestry with these 'green' chloroplasts4–6. Results from molecular sequence phytogenies, however, have suggested that _Prochlorothrix hollandica_7 is not on a lineage that leads to plastids8–12. Our results from 16S ribosomal RNA sequence comparisons, which include new sequences from the marine picoplankter Prochlorococcus mariniis_13,14 and the_Lissoclinum patella symbiont Prochloron sp.15, indicate that prochlorophytes are polyphyletic within the cyanobacterial radiation, and suggest that none of the known species is specifically related to chloroplasts. This implies that the three prochlorophytes and the green chloro-plast ancestor acquired chlorophyll b and its associated structural proteins in convergent evolutionary events. We report further that the 16S rRNA gene sequence from Prochlorococcus is very similar to those of open ocean Synechococcus strains (marine cluster A (ref. 16)), and to a family of 16S rRNA genes shotgun-cloned from plankton in the north Atlantic and Pacific Oceans17–19.

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References

  1. Cavalier-Smith, T. Biol. J. Linn. Soc. Land. 17, 289–306 (1982).
    Article Google Scholar
  2. Whitton, B. A. & Carr, N. G. in The Biology of the Cyanobacteria (eds Carr, N. G. & Whitton, B. A.) 1–8 (University of California, Berkely, 1982).
    Google Scholar
  3. Lewin, R. A. & Cheng, L. in Prochloron: a Microbial Enigma (eds Lewin, R. A. & Cheng, L. ) 1–7 (Chapman and Hall, New York, 1989).
    Google Scholar
  4. Van Valen, L. M. & Maiorana, V. C. Nature 287, 248–250 (1980).
    Article ADS CAS Google Scholar
  5. Lewin, R. A. Ann. N. Y. Acad. Sci. 361, 325–329 (1981).
    Article ADS CAS Google Scholar
  6. Margulis, L. Symbiosis in Cell Evolution (Freeman, San Francisco, 1981).
    Google Scholar
  7. Burger-Wiersma, T. et al. Int. J. Syst Bacteriol. 39, 250–257 (1989).
    Article Google Scholar
  8. Turner, S. et al. Nature 337, 380–382 (1989).
    Article ADS CAS Google Scholar
  9. Morden, C. W. & Golden, S. S. Nature 337, 382–385 (1989).
    Article ADS CAS Google Scholar
  10. Morden, C. W. & Golden, S. S. Nature 339, 400 (1989).
    Article ADS Google Scholar
  11. Morden, C. W. & Golden, S. S. J. molec. Evol. 32, 379–395 (1991).
    Article ADS CAS Google Scholar
  12. Kishino, H., Miyata, T. & Hasegawa, M. J. molec Evol. 31, 151–160 (1990).
    Article ADS CAS Google Scholar
  13. Chisholm, S. W. et al. Nature 334, 340–343 (1988).
    Article ADS Google Scholar
  14. Chisholm, S. W. et al. Archiv. Microbiol. (in the press).
  15. Lewin, R. A. & Withers, N. W. Nature 256, 735–737 (1975).
    Article ADS CAS Google Scholar
  16. Waterbury, J. B. & Rippka, R. in Bergey's Manual of Systematic Bacteriology Vol. 3 (eds Stanley, J. T. et al.) 1728–1746 (Williams and Wilkins, Baltimore, 1989).
    Google Scholar
  17. Giovannoni, S. J. et al. Nature 345, 60–62 (1990).
    Article ADS CAS Google Scholar
  18. Schmidt, T. M., DeLong, E. F. & Pace, N. R. J. Bact. 173, 4371–4378 (1991).
    Article CAS Google Scholar
  19. Britschgi, T. B. & Giovannoni, S. J. Appl. envir. Microbiol. 57, 1707–1713 (1991).
    CAS Google Scholar
  20. Lewin, R. A. Phycologia 1, 217 (1977).
    Article Google Scholar
  21. Goericke, R. & Repeta, D. Limnol. Oceanogr. (in the press).
  22. Giovannoni, S. J. et al. J. Bact. 170, 3584–3592 (1988).
    Article CAS Google Scholar
  23. Olsen, G. J. Meth. Enzym. 164, 793–838 (1988).
    Article CAS Google Scholar
  24. Swofford, D. L. Paup Version 3.0 (Illinois Natural History Survey, Champaign, Illinois, 1989).
    Google Scholar
  25. Felsenstein, J. Evolution 39, 783–791 (1985).
    Article Google Scholar
  26. Douglas, S. E. & Turner, S. J. molec. Evol. 33, 267–273 (1991).
    Article ADS CAS Google Scholar
  27. Olson, R. J., Chisholm, S. W., Zettler, E. R., Altabet, M. A. & Dusenberry, J. A. Deep Sea Res. 37, 1033–1051 (1990).
    Article ADS Google Scholar
  28. Palenik, B. & Haselkorn, R. Nature 355, 265–267 (1992).
    Article ADS CAS Google Scholar
  29. Jukes, T. H. & Cantor, C. R. in Mammalian Protein Metabolism (ed. Munro, H. N.) 21 (Academic, New York, 1969).
    Book Google Scholar
  30. Tomioka, N. & Sugiura, M. Molec. gen. Genet. 191, 45–50 (1983).
    Article Google Scholar
  31. Ohyama, K. et al. Pl. molec. Biol. Reporter 4, 148–175 (1986).
    ADS CAS Google Scholar
  32. Yang, D. et al. Proc. natn. Acad. Sci. U.S.A. 82, 4443–4447 (1985).
    Article ADS CAS Google Scholar
  33. Sambrook, J., Fritsch, E. F. & Maniatis, T. Molecular Cloning: a Laboratory Manual (Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York, 1989).
    Google Scholar
  34. Swift, H. & Robertson, D. L. Symbiosis 10, 95–113 (1991).
    Google Scholar
  35. Dzelzkalns, V. A., Szekeres, M. & Mulligan, B. J. in Plant Molecular Biology (ed. Shaw, C. H.) 277–299 (IRL. Washington DC, 1988).
    Google Scholar

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Author notes

  1. Deborah L. Robertson: Department of Molecular Genetics and Cellular Biology, University of Chicago, Chicago, Illinois 60637, USA

Authors and Affiliations

  1. Ralph M. Parsons Laboratory, 48-425 Massachusetts Institute of Technology, Cambridge, Massachusetts, 02139, USA
    Ena Urbach, Deborah L. Robertson & Sallie W. Chisholm

Authors

  1. Ena Urbach
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  2. Deborah L. Robertson
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  3. Sallie W. Chisholm
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Urbach, E., Robertson, D. & Chisholm, S. Multiple evolutionary origins of prochlorophytes within the cyanobacterial radiation.Nature 355, 267–270 (1992). https://doi.org/10.1038/355267a0

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