Abstract The mass mortality of the keystone herbivoreDiadema antillarumin the Caribbean was caused by the pathogenic ciliate from theDiadema antillarumScuticociliatosisPhilasterclade (DaScPc). Despite its confirmed pathogenicity, the environmental distribution and persistence strategies of DaScPc outside its host remain poorly understood. We used quantitative PCR, nested PCR, and Sanger sequencing across a 16-month time series and broad geographic surveys to investigate its ecological dynamics and potential environmental reservoirs. Sequencing-confirmed detections at a Florida coastal site devoid ofD. antillarumshow that DaScPc is a natural, host-independent component of the reef environment. Molecular detection on coral and macroalgal surfaces and in the plankton fraction indicates that multiple substrates can harbor the ciliate. Temporal observations revealed emerging trends with macroalgal cover and reef productivity, though no direct correlations were observed. Geographically, DaScPc was absent from outbreak sites in Panama and Réunion. Together, this data suggests spatial patchiness and a cryptic “boom-and-bust” lifestyle in which the organism persists at low abundance between outbreaks. The co-occurrence of a related nonpathogenic ciliate (Acropora/CHN/2009) further underscores the ecological complexity of thePhilasterclade. These findings broaden understanding of DaScPc ecology, confirming environmental persistence independent of its host and suggesting that parasitism may be intermittent, triggered by changing environmental conditions. This work highlights the need for higher-resolution surveillance and long-term monitoring to link ecosystem processes with the reemergence of marine disease in vulnerable coral reef systems. ImportanceThe 2022 mass mortality of the sea urchinDiadema antillarumdevastated Caribbean coral reefs, yet little is known about how the pathogenic ciliate responsible for the event persists in nature. We show that theDiadema antillarumScuticociliatosisPhilasterclade (DaScPc) occurs in reef environments even where the host(D. antillarum) is absent, indicating that it can persist independently of its host. Our findings suggest that DaScPc occupies a cryptic ecological niche within reef microbial communities and may follow a “boom–bust” dynamic, fluctuating between rare environmental states and occasional proliferation. Although direct environmental drivers remain unresolved, emerging trends with macroalgal cover and reef productivity highlight the potential influence of ecosystem conditions on ciliate abundance. This work broadens the understanding of how marine pathogens persist between outbreaks and underscores the importance of environmental surveillance for predicting and mitigating future disease events on coral reefs.
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Scuticociliate Detection and Microbiome Composition in Museum Collections of Diadema Antillarum
Abstract BackgroundThe mass mortality of the long-spined sea urchin Diadema antillarum has caused widespread ecological changes across Caribbean reefs, with recent studies identifying the etiological agent as pathogenic ciliate designated as a D. antillarum Scuticociliatosis Philaster-clade (DaScPc). The origin and ecological trajectory of DaScPc remain unresolved, raising critical questions about whether it represents a novel introduction or a resident commensal symbiont that transitioned into pathogenicity. MethodsTo address this, we tested 50 individual preserved museum specimens of D. antillarum collected between 1960 and 2020, with targeted PCR amplification of ciliate 18S, 28S, and 5.8S/ITS rRNA genes for spine, body wall, and coelomic fluid samples (n=100). Following up on recent work that identified bacterial biomarkers of DaSc, we also characterized the microbial communities associated with these museum specimens using 16S rRNA amplicon sequencing. Results. Our results reveal the presence of identical DaScPc 18S rRNA sequences in 21% of tested samples, 28S rRNA PCR yielded sequences at 96-98 % nt identity in only 2% of the tested samples, and we got no amplification from the 5.8S/ITS region. While these findings suggest possible long-term persistence or repeated emergence of this ciliate, the lack of 28S rRNA matches and lack of detection of ITS2 demonstrates that DaScPc 18S rRNA gene detections may be false positives for the ciliate over a highly conserved rRNA region. The microbial composition of the samples didn’t yield any of the previously identified disease-associated bacterial biomarkers and showed large shifts in the overall microbial community based on collection period and the facility where the samples are housed. This study demonstrates that museum-preserved echinoderm tissues retain ecologically informative microbial DNA and establishes a molecular framework for disentangling pathogen provenance and its caveats. It also highlights the value and limitations of natural history collections in reconstructing marine disease ecology.
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- Award ID(s):
- 2049225
- PAR ID:
- 10661357
- Publisher / Repository:
- bioRxiv
- Date Published:
- Format(s):
- Medium: X
- Institution:
- Cornell University
- Sponsoring Org:
- National Science Foundation
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