Photosynthetic Organelles in Dinoflagellates Derived from Other Protists

In addition to the peridinin-plastids discussed on the Dinoflagellates branch page, photosynthetic organelles in dinoflagellates include the following:

• Haptophyte-derived plastids: In the haptophore clade (Karenia, Karlodinium, Takayama) photosynthetic organelles represent real plastids - genes for many of their photosynthetic proteins have been shown to be encoded in the cell’s nucleus (Ishida and Green 2002, Patron et al. 2006, Nosenko et al. 2006). These type of endosymbiosis involving a secondary alga being engulfed by a eukaryote, is called ‘tertiary endosymbiosis’ (see Chromalveolate introductory page). Dinophysis mitra takes a haptophyte as kleptochloroplast (Koike et al. 2005).
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• Prasinophyte-derived ‘plastids’: Permanent green chloroplasts in the genus Lepidodinium (Watanabe et al. 1991, Elbrächter and Schnepf 1996, Hansen et al. 2007). It is not known whether genetic material has moved from the endosymbiont into the host’s nucleus (although this seems likely).
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• Diatom-derived photosynthetic endosymbionts: Some dinoflagellate species (e.g., Durinskia baltica, Kryptoperidinium foliaceum, Peridinium quinquecorne) house nearly complete, permanent diatom endosymbionts with chloroplasts and nucleus (e.g., Dodge 1971, Horiguchi and Pienaar 1991, 1994, Schnepf and Elbrächter 1999). This makes these host cells binucleate. Diatomophore dinoflagellates are culturable, they have been kept for years in culture collections. Nevertheless, it is interesting to note that non-photosynthetic, uninucleate versions of at least some of these species also exist in the wild, suggesting that the endosymbiosis is recent. It is not known whether any genes have moved from one nucleus to the other in diatomophore species.
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• Dictyophyte-derived plastids: One dinoflagellate species (Podolampas bipes) houses complete, permanent dictyophycean endosymbionts with chloroplasts and nucleus (Schnepf and Elbrächter 1999, Schweikert and Elbrächter 2004).
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• Cryptophyte-kleptochloroplasts: Most species of the genus Dinophysis harbour either complete cryptomonads or just their plastids (Schnepf and Elbrächter 1988, 1999, Janson 2004).

References

Dodge, J. D. 1971. A dinoflagellate with both a mesokaryotic and a eukaryotic nucleus. I. Fine structure of the nuclei. Protoplasma 73:145-157.

Dodge, J. D., and R. M. Crawford. 1971. A fine-structural survey of dinoflagellate pyrenoids and food-reserves. Bot. J. Linn. Soc. 64:105-115.

Elbrächter, M., and E. Schnepf. 1996. Gymnodinium chlorophorum, a new green, bloom-forming dinoflagellate (Gymnodiniales, Dinophyceae) with a vestigial prasinophyte endosymbiont. Phycologia 35:381-393.

Hansen, G., L. Botes, and M. de Salas. 2007a. Ultrastructure and large subunit rDNA sequences of Lepidodinium viride reveal a close relationship to Lepidodinium chlorophorum comb. nov. (= Gymnodinium chlorophorum). Phycol. Res. 55:25-41.

Horiguchi, T., and R. N. Pienaar. 1991. Ultrastructure of a marine dinoflagellate Peridinium quinquecorne Abé (Peridiniales) from South Africa with particular reference to its crysophyte endosymbiont. Bot. Mar. 34:123-131.

Horiguchi, T., and R. N. Pienaar. 1994. Ultrastructure of a new marine sand-dwelling dinoflagellate, Gymnodinium quadrilobatum sp. nov. (Dinophyceae) with special reference to its endosymbiotic alga. Europ. J. Phycol. 29:237-245.

Ishida, K., and B. R. Green. 2002. Second- and third-hand chloroplasts in dinoflagellates: phylogeny of oxygen-evolving enhancer 1 (PsbO) protein reveals replacement of a nuclear-encoded plastid gene by that of a haptophyte tertiary endosymbiont. Proc. Nat. Acad. Sci. USA 99:9294-9299.

Janson, S. 2004. Molecular evidence that plastids in the toxin-producing dinoflagellate genus Dinophysis originate from the free-living cryptophyte Teleaulax amphioxeia. Environm. Microbiol. 6:1102-1106.

Koike, K., H. Sekiguchi, A. Kobiyama, K. Takishita, M. Kawachi, K. Koike, and T. Ogata. 2005. A novel type of kleptoplastidy in Dinophysis (Dinophyceae): presence of a haptophyte-type plastid in Dinophysis mitra. Protist 156:225-237.

Nosenko, T., K. L. Lidie, F. M. Van Dolah, E. Lindquist, J. F. Cheng, and D. Bhattacharya. 2006. Chimeric plastid proteome in the Florida red tide dinoflagellate Karenia brevis. Mol. Biol. Evol. 23:2026-2038.

Patron, N. J., R. F. Waller, and P. J. Keeling. 2006. A tertiary plastid uses genes from two endosymbionts. J. Mol. Biol. 357:1373-1382.

Schnepf, E., and M. Elbrächter. 1988. Cryptophycean-like double-membrane-bound chloroplast in the dinoflagellate, Dinophysis Ehrenb.: evolutionary, phylogenetic and toxicological implications. Bot. Acta 101:196-203.

Schnepf, E., and M. Elbrächter. 1999. Dinophyte chloroplasts and phylogeny-a review. Grana 38:81-97.

Schweikert, M., and M. Elbrächter. 2004. First ultrastructural investigations of the consortium between a phototrophic eukaryotic endosymbiont and Podolampas bipes (Dinophyceae). Phycologia 43:614-623.

Watanabe, M. M., T. Sasa, S. Suda, I. Inouye, and S. Takishi. 1991. Major carotenoid composition of an endosymbiont in a green dinoflagellate, Lepidodinium viride. J. Phycol. 27:75.