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MBE Advance Access published online on March 2, 2005
Molecular Biology and Evolution, doi:10.1093/molbev/msi118
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© The Author 2005. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution. All rights reserved. For permissions, please e-mail: journals.permissions@oupjournals.org
Received February 21, 2005

Research Article

Tertiary Endosymbiosis Driven Genome Evolution in Dinoflagellate Algae

Hwan Su Yoon 1, Jeremiah D. Hackett 1, Frances M. Van Dolah 2, Tetyana Nosenko 1, Kristy L. Lidie 2, and Debashish Bhattacharya 1*

1 Department of Biological Sciences and Roy J. Carver Center for Comparative Genomics, University of Iowa, 312 Biology Building, Iowa City, Iowa 52242, USA
2 Biotoxins Program, NOAA National Ocean Service, Center for Coastal Environmental Health and Biomolecular Research, Charleston, South Carolina 29412, USA

* To whom correspondence should be addressed.
Debashish Bhattacharya, E-mail: dbhattac{at}blue.weeg.uiowa.edu


  Abstract

Dinoflagellates are important aquatic primary producers and cause "red tides". The most widespread plastid (photosynthetic organelle) in these algae contains the unique accessory pigment peridinin. This plastid putatively originated via a red algal secondary endosymbiosis and has some remarkable features, the most notable being a genome that is reduced to 1-3 gene minicircles with about 14 genes (out of an original 130-200) remaining in the organelle and a nuclear-encoded proteobacterial Form II Rubisco. The "missing" plastid genes are relocated to the nucleus via a massive transfer unequaled in other photosynthetic eukaryotes. The fate of these characters is unknown in a number of dinoflagellates that have replaced the peridinin plastid through tertiary endosymbiosis. We addressed this issue in the fucoxanthin dinoflagellates (e.g., Karenia brevis) that contain a captured haptophyte plastid. Our multiprotein phylogenetic analyses provide robust support for the haptophyte plastid replacement and are consistent with a red algal origin of the chromalveolate plastid. We then generated an expressed sequence tag (EST) database of 5,138 unique genes from K. brevis and searched for nuclear genes of plastid function. The EST data indicate the loss of the ancestral peridinin plastid characters in K. brevis including the transferred plastid genes and Form II Rubisco. These results underline the remarkable ability of dinoflagellates to remodel their genomes through endosymbiosis and the considerable impact of this process on cell evolution.

Keywords: chromalveolates; dinoflagellates; EST; Karenia brevis; minicircle genes; tertiary endosymbiosis.
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