Environmental distribution of coral-associated relatives of apicomplexan parasites

Abstract

A lineage of plastid-bearing eukaryotic microbes that is closely related to apicomplexan parasites was recently found in a specific association with coral reefs (apicomplexan-related lineage-V, or ARL-V). Here, we address the possible nature of this association using plastid 'contamination' in fine-scale bacterial sequence surveys. In a transect between corals and associated macroalgae, ARL-V is specifically associated with the coral, in contrast to all microalgal types (including diatoms, haptophytes, pelagophytes and photosynthetic apicomplexan relatives, Chromera and Vitrella), which are associated with macroalgae. ARL-V is associated with at least 20 species of symbiotic corals through extended time periods and large geographic distances. It is significantly enriched in healthy coral tissue and shallow reef depths. Altogether, the evidence points to a specific relationship between ARL-V and corals, and is suggestive of symbiosis, perhaps based on photosynthesis.

Figure 1

The fine-scale distribution of ARL-V on coral surfaces (a), between coral species (b) and across depth gradients (c). (a) Relative occurrences of plastid sequences in a five-zone transect between Montastraea annularis and associated macroalgae. Colored lines connect median values from four transects in each zone (ARLs highlighted by thicker lines). Detailed zone descriptions are in the text. T/S=tissue/surface area (b) Relative occurrence of ARL-V among seven coral species and surrounding reef water. Species compared are Montastraea faveolata (Mfa), M. franksi (Mfr), Diploria strigosa (Dst), Acropora palmata (Apa), A. cervicornis (Ace), Porites asteroides (Pas), Gorgonia ventalina (Gve). Bars indicate proportion of ARL-V sequences (as %) compared with all other sequences characterized. Numbers next to bars indicate absolute sequence counts of V6-tags, or Sanger reads (in brackets if available). Colors and colored boxes on the left indicate three distinct coral groups (S=scleractinian robust and complex clade; O=gorgonian octocoral). (c) Depth distribution of ARL-V in Montastraea annularis from 5 m, 10 m and 20 m depths. Graphs show relative occurrence of ARL-V (as %) in clone libraries compared with all other sequences characterized. A similar pattern was observed in the terminal restriction fragment length polymorphisms analysis (Klaus et al., 2007).