Jeremiah D Hackett

PMID: 12172008;PMCID: PMC129336;Abstract:

The most widely distributed dinoflagellate plastid contains chlorophyll c2 and peridinin as the major carotenoid. A second plastid type, found in taxa such as Karlodinium micrum and Karenia spp., contains chlorophylls c1 + c2 and 19′-hexanoyloxy-fucoxanthin and/or 19′-butanoyloxy-fucoxanthin but lacks peridinin. Because the presence of chlorophylls c1 + c2 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 c1 + c2 and fucoxanthin, and the Form I rbcL gene are in fact the primitive (not derived, as widely believed) condition in dinoflagellates.

Many microbes cooperatively secrete extracellular products that favorably modify their environment. Consistent with social evolution theory, structured habitats play a role in maintaining these traits in microbial model systems, by localizing the benefits and separating strains that invest in these products from 'cheater' strains that benefit without paying the cost. It is thus surprising that many unicellular, well-mixed microalgal populations invest in extracellular toxins that confer ecological benefits upon the entire population, for example, by eliminating nutrient competitors (allelopathy). Here we test the hypotheses that microalgal exotoxins are (1) exploitable public goods that benefit all cells, regardless of investment, or (2) nonexploitable private goods involved in cell-level functions. We test these hypotheses with high-toxicity (TOX+) and low-toxicity (TOX-) strains of the damaging, mixotrophic microalga Prymnesium parvum and two common competitors: green algae and diatoms. TOX+ actually benefits from dense populations of competing green algae, which can also be prey for P. parvum, yielding a relative fitness advantage over coexisting TOX-. However, with nonprey competitors (diatoms), TOX- increases in frequency over TOX+, despite benefiting from the exclusion of diatoms by TOX+. An evolutionary unstable, ecologically devastating public good may emerge from traits selected at lower levels expressed in novel environments.

The dinoflagellates are an ecologically important group of microbial eukaryotes that have evolved many novel genomic characteristics. They possess some of the largest nuclear genomes among eukaryotes arranged on permanently condensed liquid-crystalline chromosomes. Recent advances have revealed the presence of genes arranged in tandem arrays, trans-splicing of messenger RNAs, and a reduced role for transcriptional regulation compared to other eukaryotes. In contrast, the mitochondrial and plastid genomes have the smallest gene content among functional eukaryotic organelles. Dinoflagellate biology and genome evolution have been dramatically influenced by lateral transfer of individual genes and large-scale transfer of genes through endosymbiosis. Next-generation sequencing technologies have only recently made genome-scale analyses of these organisms possible, and these new methods are helping researchers better understand the biology and evolution of this enigmatic group of eukaryotes.

Abstract:

Photosynthetic members of the genus Dinophysis Ehrenberg contain a plastid of uncertain origin. Ultrastructure and pigment analyses suggest that the two-membrane-bound plastid of Dinophysis spp. has been acquired through endosymbiosis from a cryptophyte. However, these organisms do not survive in culture, raising the possibility that Dinophysis spp. have a transient kleptoplast. To test the origin and permanence of the plastid of Dinophysis, we sequenced plastid-encoded psbA and small subunit rDNA from single-cell isolates of D. acuminata Claparède et Lachman, D. acuta Ehrenberg, and D. norvegica Claparède et Lachman. Phylogenetic analyses confirm the cryptophyte origin of the plastid. Plastid sequences from different populations isolated at different times are monophyletic with robust support and show limited polymorphism. DNA sequencing also revealed plastid sequences of florideophyte origin, indicating that Dinophysis may be feeding on red algae.