Deep-sea corals provide new insight into the ecology, evolution, and the role of plastids in widespread apicomplexan symbionts of anthozoans

Samuel A Vohsen,Harald R Gruber-Vodicka,Nicole Dubilier,Richard P Dannenberg,Andrea M Gade,Iliana B Baums,Charles R Fisher,Eslam O Osman,Kaitlin E Anderson

doi:10.1186/s40168-020-00798-w

Abstract

BackgroundApicomplexans 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.ResultsWe 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.ConclusionsThe 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.F2zJxksEL9EUf83G36J_vHVideo abstract

Highlights

Apicomplexans are the causative agents of major human diseases such as malaria and toxoplasmosis
Plastid and mitochondrial genomes of corallicolids A 6300 bp mitogenome of apicomplexan origin was assembled from a colony of Leiopathes glaberrima collected from a depth of 450 m at site Viosca Knoll (VK) 826
We show that corallicolids are more widespread and diverse than previously thought by acquiring and analyzing samples from underrepresented taxa and habitats

Summary

Introduction

Apicomplexans are the causative agents of major human diseases such as malaria and toxoplasmosis. Two additional alveolate, phototrophic coral symbionts were discovered, which are both close relatives of apicomplexans: Chromera velia [16, 17] and Vitrella brassicaformis [18] These organisms attracted attention for their potential role as auxiliary phototrophic symbionts and for their phylogenetic position basal to apicomplexans. They have been postulated to represent a transitional lifestyle between free-living phototrophs and obligate parasites and may shed light on the evolutionary history of important parasites of humans, such as the apicomplexans Plasmodium spp. and Toxoplasma gondii [16, 19]

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