Cryptomonad algae are evolutionary chimaeras of two phylogenetically distinct unicellular eukaryotes

Article metrics

Abstract

ALTHOUGH it is widely accepted that the plastids of plants and algae originated as endosymbionts1, the details of this evolutionary process are unclear2'3. It has been proposed that in organisms whose plastids are surrounded by more than two membranes, the endosymbiont was a eukaryotic alga rather than a photosynthetic prokaryote4. The DNA-containing5 nucleomorph6 of cryptomonad algae appears to be the vestigial nucleus of such an algal endosymbiont7. Eukaryotic-type ribosomal RNA sequences have been localized to a nucleolus-like structure in the nucleomorph8. In support of the hypothesis that cryptomonads are evolutionary chimaeras of two distinct eukaryotic cells, we show here that Cryptomonas Φ contains two phylogenetically separate, nuclear-type small-subunit rRNA genes, both of which are transcriptionally active. We incorporate our rRNA sequence data into phylogenetic trees, from which we infer the evolutionary ancestry of the host and symbiont components of Cryptomonas Φ. Such trees do not support the thesis3 that chromophyte algae evolved directly from a cryp-tomonad-like ancestor.

Access options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

All prices are NET prices.

References

  1. 1

    Gray, M. W. Trends Genet. 5, 294–299 (1989).

  2. 2

    Whatley, J. M. & Whatley, F. R. New Phytol. 87, 233–247 (1981).

  3. 3

    Cavalier-Smith, T. Biol. J. Linn. Soc. 17, 289–306 (1982).

  4. 4

    Gibbs, S. P. Ann. N.Y. Acad. Sci. 391, 193–208 (1981).

  5. 5

    Ludwig, M. & Gibbs, S. P. Protoplasma 127, 9–20 (1985).

  6. 6

    Greenwood, A. D., Griffiths, H. B. & Santore, U. J. Br. Phycol. J. 12, 119 (1977).

  7. 7

    Ludwig, M. & Gibbs, S. P. Ann. N.Y. Acad. Sci. 503, 198–211 (1987).

  8. 8

    McFadden, G. I. J. Cell Sci. 95, 303–308 (1990).

  9. 9

    Sogin, M. L. in PCR Protocols. A Guide to Methods and Applications (eds Innes, M. A. et al.) 307–314 (Academic, San Diego, 1990).

  10. 10

    Neefs, J.-M., Van de Peer, Y., Henriks, L. & De Wachter, R. Nucleic Acids Res. 18 (suppl.), 2237–2247 (1990).

  11. 11

    Gray, M. W., Sankoff, D. & Cedergren, R. J. Nucleic Acids Res. 12, 5837–5852 (1984).

  12. 12

    Dahlberg, A. E. Cell 57, 525–529 (1989).

  13. 13

    Douglas, S. E. Curr. Genet. 14, 591–598 (1988).

  14. 14

    Schnare, M. N., Heinonen, T. Y. K., Young, P. G. & Gray, M. W. J. biol. Chem. 261, 5187–5193 (1986).

  15. 15

    Swofford, D. L. PAUP Version 3.0. Illinois Natural History Survey (Champagne, Illinois, 1989).

  16. 16

    Felsentein, J. PHYLIP Manual Version 3.3 (Herbarium, Univ. California, Berkeley, 1990).

  17. 17

    Saitou, N. & Nei, M. Molec. biol. Evol. 4, 406–425 (1987).

  18. 18

    Gunderson, J. H., Elwood, H. J., Ingold, A., Kindle, K. & Sogin, M. L. Proc. natn. Acad. Sci. U.S.A. 84, 5823–5827 (1987).

  19. 19

    Bhattacharya, D., Elwood, H. J., Goff, L. J. & Sogin, M. L. J. Phycol. 26, 181–186 (1990).

  20. 20

    Perasso, R., Baroin, A., Qu, L. H., Bachellerie, J. P. & Adoutte, A. Nature 339, 142–144 (1989).

  21. 21

    Cavalier-Smith, T. Prog. Phycol. Res. 4, 309–347 (1986).

  22. 22

    Sanger, F., Nicklen, S. & Coulson, A. R. Proc. natn. Acad. Sci. U.S.A. 74, 5463–5467 (1977).

  23. 23

    Maxam, A. M. & Gilbert, W. Meth. Enzym. 65, 499–560 (1980).

  24. 24

    Douglas, S. E. & Durnford, D. G. Plant molec. Biol. 13, 13–20 (1989).

  25. 25

    Bird, C. J., Rice, E. L., Murphy, C. A., Liu, Q. Y. & Ragan, M. A. Nucleic Acids Res. 18, 4023–4024 (1990).

  26. 26

    Hendriks, L. et al. System appl. Microbiol. 12, 223–229 (1989).

  27. 27

    Kimura, M. J. molec. Evol. 16, 111–120 (1980).

Download references

Author information

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Douglas, S., Murphy, C., Spencer, D. et al. Cryptomonad algae are evolutionary chimaeras of two phylogenetically distinct unicellular eukaryotes. Nature 350, 148–151 (1991) doi:10.1038/350148a0

Download citation

Further reading

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.