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MBE Advance Access originally published online on July 28, 2006
Molecular Biology and Evolution 2006 23(11):2026-2038; doi:10.1093/molbev/msl074
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© The Author 2006. 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@oxfordjournals.org

Research Articles

Chimeric Plastid Proteome in the Florida "Red Tide" Dinoflagellate Karenia brevis

Tetyana Nosenko*, Kristy L. Lidie{dagger}, Frances M. Van Dolah{dagger}, Erika Lindquist{ddagger}, Jan-Fang Cheng§, US Department of Energy–Joint Genome Institute{ddagger} and Debashish Bhattacharya*

* The Roy J. Carver Center for Comparative Genomics, Department of Biological Sciences, University of Iowa
{dagger} Marine Biotoxins Program, NOAA National Ocean Service, Center for Coastal Environmental Health and Biomolecular Research, Charleston, South Carolina
{ddagger} Department of Energy Joint Genome Institute and University of California Lawrence Berkeley National Laboratory, Walnut Creek, California
§ Genomics Division, Lawrence Berkeley National Laboratory, Berkeley, California

E-mail: debashi-bhattacharya{at}uiowa.edu.

Current understanding of the plastid proteome comes almost exclusively from studies of plants and red algae. The proteome in these taxa has a relatively simple origin via integration of proteins from a single cyanobacterial primary endosymbiont and the host. However, the most successful algae in marine environments are the chlorophyll c–containing chromalveolates such as diatoms and dinoflagellates that contain a plastid of red algal origin derived via secondary or tertiary endosymbiosis. Virtually nothing is known about the plastid proteome in these taxa. We analyzed expressed sequence tag data from the toxic "Florida red tide" dinoflagellate Karenia brevis that has undergone a tertiary plastid endosymbiosis. Comparative analyses identified 30 nuclear-encoded plastid-targeted proteins in this chromalveolate that originated via endosymbiotic or horizontal gene transfer (HGT) from multiple different sources. We identify a fundamental divide between plant/red algal and chromalveolate plastid proteomes that reflects a history of mixotrophy in the latter group resulting in a highly chimeric proteome. Loss of phagocytosis in the "red" and "green" clades effectively froze their proteomes, whereas chromalveolate lineages retain the ability to engulf prey allowing them to continually recruit new, potentially adaptive genes through subsequent endosymbioses and HGT. One of these genes is an electron transfer protein (plastocyanin) of green algal origin in K. brevis that likely allows this species to thrive under conditions of iron depletion.

Key Words: endosymbiosis • endosymbiotic gene transfer • Karenia brevis • proteome • red tide


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