Apicomplexans are a group of obligate intracellular parasites, but their retention of a relict non-photosynthetic plastid reveals that they evolved from free-living photosynthetic ancestors. The closest relatives of apicomplexans include photosynthetic chromerid algae (e.g., Chromera and Vitrella), non-photosynthetic colpodellid predators (e.g., Colpodella) and several environmental clades collectively called Apicomplexan-Related Lineages (ARLs). Here we investigate the global distribution and inferred ecology of the ARLs by expansively searching for apicomplexan-related plastid small ribosomal subunit (SSU) genes in large-scale high-throughput bacterial amplicon surveys. Searching more than 220 million sequences from 224 geographical sites worldwide revealed 94 324 ARL plastid SSU sequences. Meta-analyses confirm that all ARLs are coral reef associated and not to marine environments generally, but only a subset is actually associated with coral itself. Most unexpectedly, Chromera was found exclusively in coral biogenous sediments, and not within coral tissue, indicating that it is not a coral symbiont, as typically thought. In contrast, ARL-V is the most diverse, geographically widespread and abundant of all ARL clades and is strictly associated with coral tissue and mucus. ARL-V was found in 19 coral species in reefs, including azooxanthellate corals at depths greater than 500 m. We suggest this is indicative of a parasitic or commensal relationship, and not of photosynthetic symbiosis, further underscoring the importance of isolating ARL-V and determining its relationship with the coral host.
© 2018 Society for Applied Microbiology and John Wiley & Sons Ltd.