Investigating the influence of Diadematidae scuticociliatosis on host microbiome composition

Mass mortality of Diadematidae urchins, caused by a scuticociliate most closely related to Philaster apodigitiformis, affected the Caribbean in Spring 2022 and subsequently spread to the Eastern Mediterranean, Red Sea, and Western Indian Ocean. A key question around Diadematidae scuticociliatosis (DaSc) is whether the urchin microbiome varies between scuticociliatosis-affected and grossly normal urchins. Specimens of wild Diadema antillarum tissues collected for the initial assessment of the DaSc causative agent and during an experimental challenge performed on aquaculture-raised D. antillarum to satisfy Koch’s postulates were subject to 16S rRNA gene amplicon sequencing. Additional samples of abnormal urchins were collected from the most recent outbreak site in the Western Indian Ocean (Réunion). At reference (i.e., unaffected) sites, microbiome composition was tissue-specific, with taxa related to Kistimonas spp., Propionigenium spp., and Endozoicomonas spp. highly represented in amplicon libraries. DaSc-affected urchin amplicon libraries had lower taxonomic richness and a greater representation of taxa related to Fangia hongkongensis and Psychrobium spp. Challenge experiment amplicon libraries had similar composition, with greater representation of taxa most closely related to Photobacterium spp., Carboxylicivirga spp., and F. hongkongensis in specimens that manifested DaSc signs. Amplicon libraries sequenced from DaSc-affected Echinothrix diadema from Réunion were similar in composition to Caribbean DaSc-affected urchins. These data suggest that DaSc alters Diadematidae microbiomes, and that this variation is consistent between field-collected affected specimens from geographically disparate sites and during experimental challenge with the DaSc pathogen. It remains to be seen, from a mechanistic standpoint, how microbiome variation is driven by or affects the host-pathogen interaction.