Did the peridinin plastid evolve through tertiary endosymbiosis? A hypothesis

Abstract

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.

On the origin of chloroplasts, import mechanisms of chloroplast-targeted proteins, and loss of photosynthetic ability — review

“…The outermost (third) membrane of euglenoid plastids has the ability to fuse with vesicles budding from Golgi apparatus containing chloroplast precursor proteins (Sulli et al 1999), suggesting that it is homologous with the former phagosomal membrane and that algal plasma membrane has been lost (Cavalier-Smith 1999. Alternatively, myzocytic engulfment of algal chloroplasts (acquisition of algal cytoplasm with chloroplasts but not the whole algal cell; see Gibbs 1978;Tengs et al 2000;Bodył 2005;Bodył and Moszczyński 2006) by the ancestor of plastid-bearing euglenids may have resulted directly in plastids bounded by three membranes without any need to infer subsequent membrane loss.…”

Endosymbiosis and Eukaryotic Cell Evolution

“…The alternative view is that subsequent to a single red algal secondary endosymbiosis, perhaps in an ancestor of cryptophyte algae, one or more cryptic 'tertiary' endosymbiotic events served to spread this red algal-derived plastid further afield (e.g., [101][102][103][104]). This model takes into account discrepancies between the host-and organelle-associated features of the organisms in question, including the relative strength of phylogenetic signals in their nuclear, mitochondrial and plastid genomes [105].…”

The Life History and Cell Cycle of Kryptoperidinium foliaceum, A Dinoflagellate with Two Eukaryotic Nuclei

“…Their secondary plastid, called the peridinin plastid, is distinguished by the pigment peridinin and by three bounding membranes rather than the four common to most secondary plastids (see Falkowski et al 2004;Yoon et al 2005 for a review). However, other hypotheses suggest that the peridinin plastid evolved from a heterokont alga through a tertiary endosymbiosis (Body" and Moszczyń ski 2006). Dinoflagellates are unique among eukaryotic algae in that they have taken the process of endosymbiosis one step further, since in several independent lineages the peridinin plastid has been replaced either with a successive secondary plastid or with a plastid from another secondary alga, resulting in tertiary plastids.…”