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Abstract Mass mortality of the dominant coral reef herbivore Diadema antillarum in the Caribbean in the early 1980s contributed to a persistent phase shift from coral- to algal-dominated reefs. In 2022, a scuticociliate most closely related to Philaster apodigitiformis caused further mass mortality of D. antillarum across the Caribbean, leading to >95% mortality at affected sites. Mortality was also reported in the related species Diadema setosum in the Mediterranean in 2022, though the causative agent of the Mediterranean outbreak has not yet been determined. In April 2023, mass mortality of Diadema setosum occurred along the Sultanate of Oman's coastline. Urchins displayed signs compatible with scuticociliatosis including abnormal behavior, drooping and loss of spines, followed by tissue necrosis and death. Here we report the detection of an 18S rRNA gene sequence in abnormal urchins from Muscat, Oman, that is identical to the Philaster strain responsible for D. antillarum mass mortality in the Caribbean. We also show that scuticociliatosis signs can be elicited in Diadema setosum by experimental challenge with the cultivated Philaster strain associated with Caribbean scuticociliatosis. These results demonstrate the Philaster sp. associated with D. antillarum mass mortality has rapidly spread to geographically distant coral reefs, compelling global-scale awareness and monitoring for this devastating condition through field surveys, microscopy, and molecular microbiological approaches, and prompting investigation of long-range transmission mechanisms.
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Investigating the influence of Diadematidae scuticociliatosis on host microbiome composition
ABSTRACT Mass mortality of Diadematidae urchins, caused by theDiadema antillarumscuticociliatosis Philaster clade (DScPc),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 (DSc), the disease caused by the scuticociliate, is whether the urchin microbiome varies between scuticociliatosis-affected and grossly normal urchins. Tissue samples from both grossly normal and abnormalDiadema antillarumwere collected in the field during the initial assessment of the DSc causative agent and from an experimental challenge of DScPc culture on aquaculturedD. antillarum. Specimens were analyzed using 16S rRNA gene amplicon sequencing. Additional abnormal urchin samples were collected from the most recent outbreak site in the western Indian Ocean (Réunion Island). At reference (i.e., unaffected by DSc) sites,Kistimonasspp., Propionigeniumspp., andEndozoicomonasspp. were highly represented in amplicon libraries. DSc-affected urchin amplicon libraries had lower taxonomic richness and a greater representation of taxa related toFangia hongkongensisandPsychrobiumspp. Amplicon libraries of urchins experimentally challenged with the DSc pathogen had some shifts in microbial composition, butF. hongkongensiswas not a part of the core bacteria in DSc-challenged specimens. DSc-affectedEchinothrix diademafrom Réunion Island showed a similar high representation ofF. hongkongensisas that seen on CaribbeanD. antillarum. Our results suggest that DSc altersDiadematidaemicrobiomes and thatF. hongkongensismay be a candidate bacterial biomarker for DSc in environmental samples. The mechanism driving microbiome variation in host–pathogen interactions remains to be explored.IMPORTANCEThe mass mortality of Diadematidae urchins due toDiadema antillarumscuticociliatosis (DSc) has had significant ecological impacts, spreading from the Caribbean to the eastern Mediterranean, Red Sea, and western Indian Ocean. This study investigates whether the microbiome of urchins varies between those affected by DSc and those that are not. Using 16S rRNA gene amplicon sequencing, researchers found that DSc-affected urchins had lower taxonomic richness and a greater representation ofFangia hongkongensisandPsychrobiumspp. The findings indicate thatF. hongkongensiscould serve as a bacterial biomarker for DSc in environmental samples, providing a potential tool for early detection and management of the disease. Understanding these microbiome changes is crucial for developing strategies to mitigate the spread and impact of DSc on marine ecosystems.
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- Award ID(s):
- 2049225
- PAR ID:
- 10661359
- Author(s) / Creator(s):
- ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; more »
- Editor(s):
- Raina, Jean-Baptiste
- Publisher / Repository:
- mSystems
- Date Published:
- Journal Name:
- mSystems
- Volume:
- 10
- Issue:
- 3
- ISSN:
- 2379-5077
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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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.more » « less
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- Journal Article:
- https://doi.org/10.1128/msystems.01418-24
