Did some red alga‐derived plastids evolve via kleptoplastidy? A hypothesis

Abstract

The evolution of plastids has a complex and still unresolved history. These organelles originated from a cyanobacterium via primary endosymbiosis, resulting in three eukaryotic lineages: glaucophytes, red algae, and green plants. The red and green algal plastids then spread via eukaryote-eukaryote endosymbioses, known as secondary and tertiary symbioses, to numerous heterotrophic protist lineages. The number of these horizontal plastid transfers, especially in the case of red alga-derived plastids, remains controversial. Some authors argue that the number of plastid origins should be minimal due to perceived difficulties in the transformation of a eukaryotic algal endosymbiont into a multimembrane plastid, but increasingly the available data contradict this argument. I suggest that obstacles in solving this dilemma result from the acceptance of a single evolutionary scenario for the endosymbiont-to-plastid transformation formulated by Cavalier-Smith & Lee (1985). Herein I discuss data that challenge this evolutionary scenario. Moreover, I propose a new model for the origin of multimembrane plastids belonging to the red lineage and apply it to the dinoflagellate peridinin plastid. The new model has several general and practical implications, such as the requirement for a new definition of cell organelles and in the construction of chimeric organisms.

Explaining the Origin of Three‐Membrane‐Bound Plastids in Dinoflagellates and Euglenophytes: Kleptoplastidy via Myzocytosis?

“…However, such a scenario would not explain how a heterotrophic host initially became photosynthetic but, in case of dinoflagellates, rather would provide an explanation for a potential split of the dinoflagellate lineage from other alveolates by a probably accidental replacement of the secondary red plastid in the photosynthetic common ancestor of dinoflagellates and apicomplexans (Figure ). Alternatively, although not completely in agreement with more recent phylogenetic calculations (as described in), loss of one of the four plastid membranes in a dinoflagellate/apicomplexan progenitor has led to the evolution of three membrane‐bound peridinin‐containing dinoflagellate plastids (Figure ). In contrast to dinoflagellates, indications of a photosynthetic past of the euglenophyte host that acquired the three membrane‐bound plastid are, according to our knowledge, absent.…”

“…This situation would in fact be rather unlikely unless the host would already be in possession of a plastid of the same or similar type (replacement; see later). However, admittedly, when we were discussing myzocytosis in the light of dinoflagellate and euglenophyte plastid evolution, we did not consider karyoklepty that might occur in parallel to kleptoplasty as a potential consequence of myzocytosis …”

“…Dinoflagellates containing tertiary and/or kleptoplastids have been omitted from the figure for simplicity. The structure/content of the figure is based on data from Refs . and .…”

The complete chloroplast and mitochondrial genomes of the diatomNitzschia palea(Bacillariophyceae) demonstrate high sequence similarity to the endosymbiont organelles of the dinotomDurinskia baltica

“…). It is also possible secondary plastids arose by kleptoplastidy with no nucleomorph stage (Bodyl ). Later, individual stramenopile algae may have been taken up by other eukaryotic lineages, including some dinoflagellates, creating a tertiary plastid (reviewed in Burki ).…”

Microbial Diversity in the Eukaryotic SAR Clade: Illuminating the Darkness Between Morphology and Molecular Data

“…[26,101,102,115] The distribution of plastids among SAR requires multiple gains and losses. Several hypotheses have emerged that invoke primary, secondary, and even tertiary transfers of the red algal secondary plastid, [116][117][118][119][120][121] but few have generated unified support. It seems likely that the common ancestor of dinoflagellates and apicomplexan was equipped with a plastid, despite the fact that many dinoflagellates are not photosynthetic.…”