Ocean-scale transcriptomic analysis of corallicolids (Apicomplexa) reveals their ubiquity and molecular interactions with Pocillopora corals.

Corals are complex holobionts, encompassing numerous prokaryotes, viruses, and protists. This associated microbial community strongly influences coral health and its resilience to global ocean warming. Corallicolid apicomplexans are widespread coral-infecting parasites, yet their impact on the coral host remains poorly understood. This knowledge gap largely stems from the low abundance of these parasites in coral tissues, which makes them difficult to isolate and access to their genetic material. Here we analyzed nearly 1,000 Pocillopora coral colonies collected from 32 islands during the Tara Pacific expedition to identify the drivers of corallicolid prevalence and abundance. Corallicolids were detected in almost all Pocillopora colonies with variable relative abundances between islands. The high abundance of specific corallicolid populations correlates with seawater temperature and levels of host protein carbonylation. We used a large collection of 297 metatranscriptomes to assemble a corallicolid transcriptome and we identified apicomplexan parasite signature genes, including the GRA9 and PV2 confirming the close phylogenetic relationship with the family of Eimeriidae. Gene expression patterns indicate that the high abundance of corallicolids correlates with a high transcription of genes encoding apical complex proteins and genes involved in the control of host immune defenses. Overall, this study provides new insights into corallicolid biology and its interaction with the coral host by combining a newly generated transcriptome with a large-scale sampling of Pocillopora corals across the Pacific Ocean.