Host-independent persistence of the Diadema antillarum Scuticociliatosis Philaster clade in coastal environments

Abstract

The mass mortality of the keystone herbivore Diadema antillarum in the Caribbean was caused by the pathogenic ciliate from the Diadema antillarum Scuticociliatosis Philaster clade (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 of D. antillarum show 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 Reunion. 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 the Philaster clade. 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 urchin Diadema antillarum devastated Caribbean coral reefs, yet little is known about how the pathogenic ciliate responsible for the event persists in nature. We show that the Diadema antillarum Scuticociliatosis Philaster clade (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.