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Background Apicomplexans are the causative agents of major human diseases such as malaria and toxoplasmosis. A novel group of apicomplexans, recently named corallicolids, have been detected in corals inhabiting tropical shallow reefs. These apicomplexans may represent a transitional lifestyle between free-living phototrophs and obligate parasites. To shed light on the evolutionary history of apicomplexans and to investigate their ecology in association with corals, we screened scleractinians, antipatharians, alcyonaceans, and zoantharians from shallow, mesophotic, and deep-sea communities. We detected corallicolid plastids using 16S metabarcoding, sequenced the nuclear 18S rRNA gene of corallicolids from selected samples, assembled and annotated the plastid and mitochondrial genomes from a corallicolid that associates with a deep-sea coral, and screened the metagenomes of four coral species for corallicolids. Results We detected 23 corallicolid plastotypes that were associated with 14 coral species from three orders and depths down to 1400 m. Individual plastotypes were restricted to coral hosts within a single depth zone and within a single taxonomic order of corals. Some clusters of closely related corallicolids were revealed that associated with closely related coral species. However, the presence of divergent corallicolid lineages that associated with similar coral species and depths suggests that corallicolid/coral relations are flexible over evolutionary timescales and that a large diversity of apicomplexans may remain undiscovered. The corallicolid plastid genome from a deep-sea coral contained four genes involved in chlorophyll biosynthesis: the three genes of the LIPOR complex and acsF. Conclusions The presence of corallicolid apicomplexans in corals below the photic zone demonstrates that they are not restricted to shallow-water reefs and are more general anthozoan symbionts. The presence of LIPOR genes in the deep-sea corallicolid precludes a role involving photosynthesis and suggests they may be involved in a different function. Thus, these genes may represent another set of genetic tools whose function was adapted from photosynthesis as the ancestors of apicomplexans evolved towards parasitic lifestyles.
