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Cryptophyte algae are robbed of their organelles by the marine ciliate Mesodinium rubrum

Nature volume 405, pages 1049–1052 (2000)Cite this article

Abstract

Mesodinium rubrum (Lohmann 1908) Jankowski 1976 (= Myrionecta rubra)1,2 is a common photosynthetic marine planktonic ciliate which can form coastal red-tides3. It may represent a ‘species complex’4,5 and since Darwin's voyage on the Beagle, it has been of great cytological, physiological and evolutionary interest4. It is considered to be functionally a phytoplankter because it was thought to have lost the capacity to feed and possesses a highly modified algal endosymbiont5,6. Whether M. rubrum is the result of a permanent endosymbiosis or a transient association between a ciliate and an alga is controversial7. We conducted ‘feeding’ experiments to determine how exposure to a cryptophyte alga affects M. rubrum. Here we show that although M. rubrum lacks a cytostome (oral cavity)8, it ingests cryptophytes and steals their organelles, and may not maintain a permanent endosymbiont. M. rubrum does not fall into recognized cellular or functional categories, but may be a chimaera partially supported by organelle robbery.

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Figure 1: Changes in Mesodinium rubrum and cryptophyte populations measured by flow cytometry.
Figure 2: Ingestion of cryptophytes by M. rubrum when exposed to about 104 cryptophytes ml-1 after not being fed for 14 days.
Figure 3: Chlorophyll content per cell and photosynthetic performance of M. rubrum at 10 and 17 days after addition of cryptophytes.

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References

  1. Small, E. B. & Lynn, D. H. in Illustrated Guide to the Protozog (eds Lee, J. J., Hunter, S. H. & Bovee, E. C.) 393– 575 (Allen Press, Kansas, 1985).

  2. Krainer, K. -H. & Foissner, W. Revision of the genus Askenasia Blochmann, 1895, with proposal of two new species, and description of Rhabdoaskenasia minima N. G., N. Sp. (Ciliophora, Cyclotrichida). J. Protozool. 37, 414 –427 (1990).

    Article  Google Scholar 

  3. Montagnes, D. J. S. & Lynn, D. H. The annual cycle of Mesodinium rubrum in the waters surrounding the Isles of Shoals, Gulf of Maine. J. Plank. Res. 11, 193– 201 (1989).

    Article  Google Scholar 

  4. Lindholm, T. in Advances in Aquatic Microbiology. Vol. 3 (eds Jannasch, H. W. & Williams, P. J.) 1–48 (Academic, London 1985).

    Google Scholar 

  5. Crawford, D. W. Mesodinium rubrum: the phytoplankter that wasn't. Mar. Ecol. Prog. Ser. 58, 161–174 ( 1989).

    Article  ADS  Google Scholar 

  6. Oakley, B. R. & Taylor, F. J. R. Evidence for a new type of endosymbiotic organization in a population of the ciliate Mesodinium rubrum from British Columbia. BioSystems 10, 361–369 (1978).

    Article  CAS  Google Scholar 

  7. Hibberd, D. J. Observations on the ultrastructure of the cryptomonad endosymbiont of the red-water ciliate Mesodinium rubrum. J. Mar. Biol. Assoc. UK 57, 45–61 ( 1977).

    Article  Google Scholar 

  8. Lindholm, T., Lindroos, P. & Mörk, A.-C. Ultrastructure of the photosynthetic ciliate Mesodinium rubrum. BioSystems 21, 141 –149 (1988).

    Article  CAS  Google Scholar 

  9. Taylor, F. J. R., Blackbourn, D. J. & Blackbourn, J. The red-water ciliate Mesodinium rubrum and its “incomplete symbionts”: a review including new ultrastructural observations. J. Fish. Res. Bd Can. 28, 391–407 (1971).

    Article  Google Scholar 

  10. Barber, R. T., White, A. W. & Siegelman, H. W. Evidence for a cryptomonad symbiont in the ciliate, Cyclotrichium meunieri. J. Phycol. 5, 86–88 (1969).

    Article  CAS  Google Scholar 

  11. Laval-Peuto, M., Salvano, P., Gayol, P. & Gruet, C. Mixotrophy in marine planktonic ciliates: ultrastructure study of Tontonia appendiculariformis (Ciliophora, Oligotrichina). Mar. Microb. Food Webs 1, 81–104 (1986).

    Google Scholar 

  12. Stoecker, D. K. & Silver, M. W. Replacement and aging of chloroplasts in Strombidium capitatum (Ciliophora:Oligotrichida). Mar. Biol. 107, 491–502 (1990).

    Article  Google Scholar 

  13. Lindholm, T. & Mörk, A.-C. Symbiotic algae and plastids in planktonic ciliates. Mem. Soc. Fauna Flora Fennica 65, 17–22 (1989).

    Google Scholar 

  14. Hargraves, P. Narrow River phytoplankton. Maritimes 35, 6–8 (1991).

    Google Scholar 

  15. Packard, T. T., Blasco, D. & Barber, R. T. in Upwelling Ecosystems (eds Boje, R. & Tomczak, M.) 73–89 (Springer, New York, 1978).

    Book  Google Scholar 

  16. Crawford, D. W., Purdie, D. A., Lockwood, A. P. M. & Weissman, P. Recurrent red-tides in the Southampton Water estuary caused by the phototrophic ciliate Mesodinium rubrum. Est. Coast. Shelf Sci. 45, 799–812 (1997).

    Article  ADS  CAS  Google Scholar 

  17. Smith, W. O. & Barber, R. T. A carbon budget for the autrophic ciliate Mesodinium rubrum. J. Phycol. 15, 27–33 (1979).

    Article  Google Scholar 

  18. Wilkerson, F. P. & Grunseich, G. Formation of blooms by the symbiotic ciliate Mesodinium rubrum: the significance of nitrogen uptake. J. Plank. Res. 12, 973 –989 (1990).

    Article  Google Scholar 

  19. Kifle, D. & Purdie, D. A. The seasonal abundance of the phototrophic ciliate Mesodinium rubrum in Southampton Water, England. J. Plank. Res. 15, 823– 833 (1993).

    Article  Google Scholar 

  20. Stoecker, D. K., Taniguchi, A. & Michaels, A. E. Abundance of autotrophic, mixotrophic and heterotrophic planktonic ciliates in shelf and slope waters. Mar. Ecol. Prog. Ser. 50, 241–254 ( 1989).

    Article  ADS  Google Scholar 

  21. Stoecker, D. K., Putt, M., Davis, L. H. & Michaels, A. E. Photosynthesis in Mesodinium rubrum: species-specific measurements and comparison to community rates. Mar. Ecol. Prog. Ser. 73, 245–252 (1991).

    Article  ADS  Google Scholar 

  22. Sanders, R. W. Seasonal distributions of the photosynthesizing ciliates Laboea strobila and Myrionecta rubra (= Mesodinium rubrum) in an estuary of the Gulf of Maine. Aquatic Microb. Ecol. 9, 237–242 (1995).

    Article  Google Scholar 

  23. Crawford, D. W. & Lindholm, T. Some observations on vertical distribution and migration of the phototrophic ciliate Mesodinium rubrum (= Myrionecta rubra) in a stratified brackish inlet. Aquatic Microb. Ecol. 13, 267–274 (1997).

    Article  Google Scholar 

  24. Yih, W. & Shim, J. H. The planktonic phototrophic ciliate, Mesodinium rubrum, as a useful organism for marine biotechnological applications. J. Mar. Biotechnol. 5, 82– 85 (1997).

    Google Scholar 

  25. Stoecker, D. K. in Protozoa and Their Role in Marine Processes Vol. G 25 (eds Reid, P. C. et al.) 161–179 (NATO ASI Series, Springer, Berlin–Heidelberg, 1991).

    Book  Google Scholar 

  26. Stoecker, D. K., Michaels, A. E. & Davis, L. H. Large proportion of marine planktonic ciliates found to contain functional chloroplasts. Nature 326, 790–792 (1987).

    Article  ADS  Google Scholar 

  27. White, A. W., Sheath, R. G. & Hellebust, J. A. A red tide caused by the marine ciliate Mesodinium rubrum in Passamaquoddy Bay, including pigment and ultrastructure studies of the endosymbiont. J. Fish. Res. Bd Can. 34, 413–416 (1977).

    Article  Google Scholar 

  28. Stoecker, D. K., Silver, M. W., Michaels, A. E. & Davis, L. H. Obligate mixotrophy in Laboea strobila, a ciliate which retains chloroplasts. Mar. Biol. 99, 415–423 (1988).

    Article  Google Scholar 

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Acknowledgements

We thank P. Del Giorgio for discussions; D. W. Coats, P. Krugens and G. Sellers for taxonomic assistance; and A. Li for isolating the cryptophyte. This work was partially supported by the US NSF Polar and Biological Oceanography (D.K.S.) and Maryland Sea Grant (K.S.).

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  1. University of Maryland, Center for Environmental Science, Horn Point Laboratory, PO Box 775, Cambridge, 21613, Maryland, USA

    Daniel E. Gustafson Jr, Diane K. Stoecker, Matthew D. Johnson, William F. Van Heukelem & Kerri Sneider

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Correspondence to Daniel E. Gustafson Jr.

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Gustafson, D., Stoecker, D., Johnson, M. et al. Cryptophyte algae are robbed of their organelles by the marine ciliate Mesodinium rubrum. Nature 405, 1049–1052 (2000). https://doi.org/10.1038/35016570

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