Dinoflagellate protists harbor a characteristic peridinin-containing plastid that evolved from a red or haptophyte alga. In contrast to typical plastids that have ∼100-200 kb circular genomes, the dinoflagellate plastid genome is composed of minicircles that each encode 0-5 genes. It is commonly assumed that dinoflagellate minicircles are derived from a standard plastid genome through drastic reduction and fragmentation. However, we demonstrate that the ycf16 and ycf24 genes (encoded on the Ceratium AF490364 minicircle), as well as rpl28 and rpl33 (encoded on the Pyrocystis AF490367 minicircle), are related to sequences from Algoriphagus and/or Cytophaga bacteria belonging to the Bacteroidetes clade. Moreover, we identified a new open reading frame on the Pyrocystis minicircle encoding a SRP54 N domain, which is typical of FtsY proteins. Because neither of these minicircles share sequence similarity with any other dinoflagellate minicircles, and their genes resemble bacterial operons, we propose that these Ceratium and Pyrocystis minicircles resulted from a horizontal gene transfer (HGT) from a Bacteroidetes donor. Our findings are the first indication of HGT to dinoflagellate minicircles, highlighting yet another peculiar aspect of this plastid genome.
Most photosynthetic dinoflagellates harbour the peridinin plastid. This plastid is surrounded by three membranes and its characteristic pigments are chlorophyll c and the carotenoid peridinin. The evolutionary origin of this peculiar plastid remains controversial and is hotly debated. On the recently published tree of concatenated plastid-encoded proteins, dinoflagellates emerge from within the Chromista (clade containing cryptophytes, heterokonts, and haptophytes) and cluster specifically with Heterokonta. These data inspired a new version of the 'chromalveolate' model, according to which the peridinin plastid evolved by 'descent with modification' from a heterokont-like plastid that had been acquired from a rhodophyte by an ancestral chromalveolate. However, this model of plastid evolution encounters serious obstacles. Firstly, the heterokont plastid is surrounded by four membranes, which means that the ancestral peridinin plastid must have lost one of these primary membranes. However, such a loss could be traumatic, because it could potentially disturb protein import into and/or within the plastid. Secondly, on the phylogenetic tree of Dinoflagellata and Heterokonta, the first to diverge are not plastid, but heterotrophic, aplastidal taxa. Thus, when accepting the single origin of the heterokont and peridinin plastids, we would have to postulate multiple plastid losses, but such a scenario is highly doubtful when the numerous non-photosynthetic functions of plastids and their existence in heterotrophic protists, including parasitic lineages, are considered. Taking these obstacles into account, we suggest an alternative interpretation of the concatenated tree of plastid-encoded proteins. According to our hypothesis, the peridinin plastid evolved from a heterokont alga through tertiary endosymbiosis.
Organelle genomes lose their genes by transfer to host nuclear genomes, but only occasionally are enriched by foreign genes from other sources. In contrast to mitochondria, plastid genomes are especially resistant to such horizontal gene transfer (HGT), and thus every gene acquired in this way is notable. An exceptional case of HGT was recently recognized in the peculiar peridinin plastid genome of dinoflagellates, which is organized in plasmid-like minicircles. Genomic and phylogenetic analyses of Ceratium horridum and Pyrocystis lunula minicircles revealed four genes and one unannotated open reading frame that probably were gained from bacteria belonging to the Bacteroidetes. Such bacteria seem to be a good source of genes because close endosymbiotic associations between them and dinoflagellates have been observed. The HGT-acquired genes are involved in plastid functions characteristic of other photosynthetic eukaryotes, and their arrangement resembles bacterial operons. These studies indicate that the peridinin plastid genome, usually regarded as having resulted from reduction and fragmentation of a typical plastid genome derived from red algae, may have a chimeric origin that includes bacterial contributions. Potential contamination of the Ceratium and Pyrocystis plastid genomes by bacterial sequences and the controversial localization of their minicircles in the nucleus are also discussed.
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