Endosymbiosis and kleptoplastidy in the evolution of complex algae

Complex algae form a network of photosynthetic organisms spread across the eukaryotic tree. Among those, CASH lineages have plastids related to red algae, but the mechanisms by which they were acquired remain unclear. Contrary to expectations of secondary endosymbiotic models, a sizable part of their plastid-targeted genes is not from the same origin as the plastid itself. Scenarios as the ancestral cryptic serial endosymbioses or the shopping bag model provide a substantial interpretation of this gene mosaicism but are exclusively focusing on an endosymbiotic mechanism. Similarly, while the Rhodoplex hypothesis fits the single phylogenetic origin of complex red plastids, it does not explain gene mosaicism. Moreover, it implies multiple tertiary (or quaternary) endosymbiotic events, whereas most complex algae do not bear nucleomorphs and only have 3 or 4 membranes surrounding their plastids. To overcome the inconsistencies of those models, we propose kleptoplasty as an additional mechanism for explaining plastid spread in CASH lineages. In line with the shopping bag model, our hypothesis posits multiple transient interactions with preys of diverse origins but also proposes a rationale for the selective force driving the progressive accumulation of plastid-targeted genes: to maintain functional kleptoplastids for increasingly longer periods of time, before ultimately reducing them into fully integrated plastids. In such a scenario, the phylogenetic diversity of plastid-targeted genes would be higher than predicted with endosymbiotic models, where genes originate mostly from a single source, the algal symbiont. To test our hypothesis, we designed and implemented an automated pipeline for building and parsing gene trees in a discovery-driven and taxonomy-aware fashion. This approach allows us to infer whether any given CASH alga rather arose through endosymbiosis or kleptoplasty by reading its position on an alpha-diversity ladder, ranging from (theoretically) single-source nucleomorph-bearing organisms (e.g., Guillardia theta) to multiple-source kleptoplastic organisms (e.g., Dinophysis acuminata)