A single origin of the peridinin- and fucoxanthin-containing plastids in dinoflagellates through tertiary endosymbiosis

Abstract

The most widely distributed dinoflagellate plastid contains chlorophyll c(2) and peridinin as the major carotenoid. A second plastid type, found in taxa such as Karlodinium micrum and Karenia spp., contains chlorophylls c(1) + c(2) and 19'-hexanoyloxy-fucoxanthin and/or 19'-butanoyloxy-fucoxanthin but lacks peridinin. Because the presence of chlorophylls c(1) + c(2) and fucoxanthin is typical of haptophyte algae, the second plastid type is believed to have originated from a haptophyte tertiary endosymbiosis in an ancestral peridinin-containing dinoflagellate. This hypothesis has, however, never been thoroughly tested in plastid trees that contain genes from both peridinin- and fucoxanthin-containing dinoflagellates. To address this issue, we sequenced the plastid-encoded psaA (photosystem I P700 chlorophyll a apoprotein A1), psbA (photosystem II reaction center protein D1), and "Form I" rbcL (ribulose-1,5-bisphosphate carboxylase/oxygenase) genes from various red and dinoflagellate algae. The combined psaA + psbA tree shows significant support for the monophyly of peridinin- and fucoxanthin-containing dinoflagellates as sister to the haptophytes. The monophyly with haptophytes is robustly recovered in the psbA phylogeny in which we increased the sampling of dinoflagellates to 14 species. As expected from previous analyses, the fucoxanthin-containing dinoflagellates formed a well-supported sister group with haptophytes in the rbcL tree. Based on these analyses, we postulate that the plastid of peridinin- and fucoxanthin-containing dinoflagellates originated from a haptophyte tertiary endosymbiosis that occurred before the split of these lineages. Our findings imply that the presence of chlorophylls c(1) + c(2) and fucoxanthin, and the Form I rbcL gene are in fact the primitive (not derived, as widely believed) condition in dinoflagellates.