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A Widespread Coral-Infecting Apicomplexan with Chlorophyll Biosynthesis Genes ­Waldan K

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A Widespread Coral-Infecting Apicomplexan with Chlorophyll Biosynthesis Genes ­Waldan K LETTER https://doi.org/10.1038/s41586-019-1072-z A widespread coral-infecting apicomplexan with chlorophyll biosynthesis genes Waldan K. Kwong1*, Javier del Campo1, Varsha Mathur1, Mark J. A. Vermeij2,3 & Patrick J. Keeling1 Apicomplexa is a group of obligate intracellular parasites that obligate parasitic Apicomplexa and the free-living chromerids, which includes the causative agents of human diseases such as malaria makes them promising candidates for studying the transition between and toxoplasmosis. Apicomplexans evolved from free-living these different lifestyles. phototrophic ancestors, but how this transition to parasitism To address evolutionary questions surrounding the transitional occurred remains unknown. One potential clue lies in coral reefs, steps to parasitism, and to reconcile the currently incomparable data of which environmental DNA surveys have uncovered several on the extent of apicomplexan diversity in corals, we sampled diverse lineages of uncharacterized basally branching apicomplexans1,2. anthozoan species from around the island of Curaçao in the south- Reef-building corals have a well-studied symbiotic relationship ern Caribbean and surveyed the composition of their eukaryotic and with photosynthetic Symbiodiniaceae dinoflagellates (for example, prokaryotic microbial communities (Supplementary Table 1). From a Symbiodinium3), but the identification of other key microbial total of 43 samples that represent 38 coral species, we recovered api- symbionts of corals has proven to be challenging4,5. Here we complexan type-N 18S rRNA genes (putatively encoded by the nucleus) use community surveys, genomics and microscopy analyses to and ARL-V 16S rRNA genes (putatively encoded by the plastid) from identify an apicomplexan lineage—which we informally name 62% and 84% of samples, respectively (Fig. 1a, Supplementary Table 2). ‘corallicolids’—that was found at a high prevalence (over 80% The type-N genes were only detected in corals that were also posi- of samples, 70% of genera) across all major groups of corals. tive for ARL-V, which suggests that they come from the same organ- Corallicolids were the second most abundant coral-associated ism; the high abundance of Symbiodiniaceae probably depressed our microeukaryotes after the Symbiodiniaceae, and are therefore detection of the type-N apicomplexan. Excluding Symbiodiniaceae, core members of the coral microbiome. In situ fluorescence and type-N apicomplexans were the most common microbial eukaryote electron microscopy confirmed that corallicolids live intracellularly detected in corals, comprising 2.1% of the total sequence reads (56% within the tissues of the coral gastric cavity, and that they possess of all non-Symbiodiniaceae reads). No other apicomplexan-related lin- apicomplexan ultrastructural features. We sequenced the genome eage was present, except for six reads of Vitrella 16S rRNA in a single of the corallicolid plastid, which lacked all genes for photosystem sample. We also searched 31 publically available coral metagenomic proteins; this indicates that corallicolids probably contain a non- and metatranscriptomic datasets that collectively amount to 15.8 Gb photosynthetic plastid (an apicoplast6). However, the corallicolid of assembled sequence (Supplementary Table 3). Sequences that plastid differs from all other known apicoplasts because it retains the correspond to rRNAs from type-N and ARL-V were present in 27 and four ancestral genes that are involved in chlorophyll biosynthesis. 12 datasets, respectively (Fig. 1b); the discrepancy probably reflects Corallicolids thus share characteristics with both their parasitic and the lower copy number of plastid rRNA genes. We further identified their free-living relatives, which suggests that they are evolutionary a suite of organelle-derived protein-coding genes (see below), and intermediates and implies the existence of a unique biochemistry for each gene we found only a single apicomplexan sequence type during the transition from phototrophy to parasitism. to be predominant (Fig. 1b, Extended Data Fig. 1). All of these data Apicomplexan parasites rely on highly specialized systems to infect are consistent with the presence of a single dominant apicomplexan animal cells, live within those cells and evade host defences. Recently, lineage in corals, for which we propose the name corallicolids (meaning it has come to light that these parasites evolved from phototrophic ‘coral-dwellers’, from Latin corallium combined with the suffix –cola, ancestors. Most apicomplexans have been found to retain relict plast- derived from the Latin incola). Our results indicate that this is the sec- ids6, and two photosynthetic ‘chromerids’ (Chromera velia and Vitrella ond most abundant microeukaryote that lives in association with coral, brassicaformis) isolated from coral reef environments have been found after the Symbiondiniaceae. to be the closest free-living relatives to the parasitic Apicomplexa7–9. The high prevalence of corallicolids in wild corals is suggestive of The finding that the photosynthetic relatives of apicomplexans are a tight symbiosis (defined as two organisms that engage in long-term somehow linked to coral reefs has prompted a major re-evaluation of interactions), across a broad diversity of coral species. To test the host the ecological conditions and symbiotic associations that drove the range of this symbiosis, we analysed 102 commercial aquarium samples evolution of parasitism in this clade2,10–12. Corals (class Anthozoa) that represented at least 61 species from across the major clades have not traditionally been considered a common host for apicompl- of Anthozoa. We detected corallicolid 18S rRNA genes in 53% of exans: sporadic reports over the last 30 years include the morphological aquarium samples, including in soft-bodied octocorals, zoanthids, description of a single coccidian (Gemmocystis cylindrus) from histo- anemones and corallimorphs (Fig. 1c). Combined with existing logical sections of eight Caribbean coral species13, and the detection data from wild corals (Supplementary Table 4), corallicolids were of 18S rRNA gene sequences of apicomplexans (known as the ‘type-N’ found in 1,271 of 1,546 samples (82% prevalence) and in 43 out of apicomplexan) in Caribbean, Australian and Red Sea corals14–16. Plastid 62 host genera (70%), from all parts of the anthozoan phylogeny 16S rRNA gene surveys have also revealed that a number of uncharac- that we have examined thus far. Ecologically, the distribution of terized apicomplexan-related lineages (notably, the ‘ARL-V’ lineage) corallicolids is highly restricted: we searched large-scale 18S rRNA are closely associated with reefs worldwide1,2. These lineages appear datasets from various terrestrial and marine ecosystems (1,014 sam- to occupy a phylogenetic position that is intermediate between the ples, 837 million sequence reads), and found that type-N was almost 1Department of Botany, University of British Columbia, Vancouver, British Columbia, Canada. 2Aquatic Microbiology, Institute for Biodiversity and Ecosystem Dynamics, University of Amsterdam, 3 Amsterdam, The Netherlands. CARMABI Foundation, Willemstad, Curaçao, The Netherlands. *e-mail: [email protected] 4 APRIL 2019 | VOL 568 | NATURE | 103 RESEARCH LETTER a Caribbean (Curaçao) corals c Corallicolid prevalence Aquarium 1.0 Previous records e Anthozoa phylogeny Wild ARL-V J K2 K S T U 0.8 * 0.6 Vitrella Zoantharia 7 of (zoanthids) 11 0.4 Hexacorals 0.2 Actiniaria (sea anemones) 1 of 2 (16S rRNA gene) Plastid abundanc 0 ND *********** ******** ND ND **** ND *** *** **** Antipatharia 1.0 2 of 2 (black corals) Corallimorpharia 3 of 6 0.8 (mushroom corals) e Scleractinia, robust 25 23 24 47 9 1 of 1 (stony corals) of 43 of 25 of 24 906 of 52 of 11 0.6 of Scleractinia, complex 14 11 18 82 1,078 91 3 of 3 (stony corals) of 23 of 16 of 21 of 90 of 121 0.4 Octocorals Alcyonacea 4 (soft corals and of 16 gorgonians) (18S rRNA gene) Eukaryote abundanc 600 400 200 0 Ma ARL-V 16S Type-N 18S G. cylindrus 0.2 ***** *** * ************* ***** 0 d Corallicolid community dissimilarity Scleractinia Antipatharia Type-N Symbiodiniaceae Rhodophyta Chlorophyta Syndiniales Ciliates Other 1 b Coral metagenomes and metatranscriptomes Coral host Australia Caribbean 0 Cyphastrea Diploria Orbicella Siderastrea 2 Acropora aculeus sp. sp. sp. sp. Mycedium elephantotus –1 Type-N 18S rRNA NMDS ARL-V 16S rRNA Pachyseris speciosa Corallicolid mitochondria –2 Corallicolid plastid Chromera 18S rRNA ANOSIM: R = 0.465, P = 0.001 –3 Stress = 0.230 Vitrella 18S rRNA –1 0123 Complete genome Present Present, < 0.5× coverage Absent NMDS 1 Fig. 1 | A single apicomplexan symbiont is present in diverse corals. of contigs compared to the complete organellar genomes. c, Presence of a, Relative abundances of plastids (top) and microbial eukaryote corallicolids across the anthozoan phylogeny. Data include aquarium and communities (bottom), based on 16S and 18S rRNA gene sequencing. wild-collected samples from this study, and wild samples from previous Each column represents data from a single coral sample. The presence studies (labelled as J (ref. 11), K (ref. 23), K2 (ref. 29), S (ref. 15), T (ref. 14) of ARL-V and type-N is also denoted by asterisks (in addition to bars) and U (ref. 13)) that used various methods to detect ARL-V, type-N and/or to aid in visualization for samples in which they are present at low G. cylindrus (details in Supplementary Table 4). The coral phylogeny abundances. The 16S rRNA gene primers that we
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