Underestimated genomic footprint of kleptoplasty in complex algae evolution?

Complex algae form a network of photosynthetic organisms scattered across the eukaryotic tree. However, the exact mechanisms by which their plastids were acquired remain unclear. Contrary to expectations of secondary endosymbiotic models, a sizable part of plastid-targeted genes are not from the same origin as the plastid itself. For example, for CASH lineages (bearing complex red plastids), scenarios like the ancestral cryptic serial endosymbioses or the shopping bag model provide a possible interpretation of gene mosaicism but focus on the endosymbiotic mechanism. Similarly, while the Rhodoplex hypothesis fits the single phylogenetic origin of those 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 three or four membranes surrounding their plastids. To overcome the inconsistencies of those models, kleptoplasty was suggested as an additional mechanism for explaining plastid spread, not only in CASH lineages but also in euglenids. In line with the shopping bag model, this 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 nucleus-encoded plastid-targeted genes would be higher than predicted with the endosymbiotic models, where genes originate mostly from a single source, the algal symbiont. To test the idea, we designed and implemented an automated phylogenetic pipeline for detecting transfers in single-gene trees in a discovery-driven and taxonomy-aware fashion. By transforming individual transfer events to organism-centric alpha-diversities, this approach allowed us to quantify the relative contribution of endosymbiosis and kleptoplasty in the origin of complex algae.