The evolutionary transition from alga to parasite in the sister lineage of apicomplexans

The chrompodellids are a collection of photosynthetic "chromerids" and heterotrophic "colpodellids," which are together the sister lineage to the apicomplexans,¹ a group of parasites containing many human disease-causing agents and species of ecological and economic importance. These lineages all descend from a photosynthetic ancestor and have been a model to understand the evolutionary transition from free-living alga to obligate parasite. Only a handful of species of chrompodellids are described-most are free-living predators, while two are photosynthetic and two are parasitic.^1,2,3,4,5 The parasites evolved independently to different forms of parasitism: one is intracellular, and the other is an extracellular gut parasite. Here, we describe a third parasitic chrompodellid, Holdonia amygdala gen. nov. sp. nov., which has an entirely different strategy, being an ectoparasite on the surface of the errantid polychaete, Micropodarke. Using single-cell transcriptomics from four individual cells, phylogenomic analysis of 232 conserved genes shows H. amygdala is not specifically related to either known parasite but instead branches deep within the chrompodellids, which are distantly related to both the intracellular parasite Piridium sociabile and the photosynthetic Vitrella brassicaformis. Despite losing photosynthesis independently, the H. amygdala and P. sociabile plastid genomes have converged on a similar gene content and a non-canonical genetic code. Overall, these data suggest that these are predictable outcomes in the evolutionary transition from free-living alga to heterotrophic parasite that emerge repeatedly in parallel.