Investigating the influence of Diadematidae scuticociliatosis on host microbiome composition

ABSTRACT Mass mortality of Diadematidae urchins, caused by the Diadema antillarum scuticociliatosis 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 scuticociliat...

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Main Authors: Brayan Vilanova-Cuevas, Christopher M. DeRito, Isabella T. Ritchie, Christina A. Kellogg, James S. Evans, Alizee Zimmerman, Stacey M. Williams, Marilyn Brandt, Moriah Sevier, Samuel Gittens, Kayla A. Budd, Matthew Warham, William C. Sharp, Gabriel A. Delgado, Alwin Hylkema, Kimani Kitson-Walters, Jean-Pascal Quod, Mya Breitbart, Ian Hewson
Format: Article
Language:English
Published: American Society for Microbiology 2025-03-01
Series:mSystems
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Online Access:https://journals.asm.org/doi/10.1128/msystems.01418-24
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author Brayan Vilanova-Cuevas
Christopher M. DeRito
Isabella T. Ritchie
Christina A. Kellogg
James S. Evans
Alizee Zimmerman
Stacey M. Williams
Marilyn Brandt
Moriah Sevier
Samuel Gittens
Kayla A. Budd
Matthew Warham
William C. Sharp
Gabriel A. Delgado
Alwin Hylkema
Kimani Kitson-Walters
Jean-Pascal Quod
Mya Breitbart
Ian Hewson
author_facet Brayan Vilanova-Cuevas
Christopher M. DeRito
Isabella T. Ritchie
Christina A. Kellogg
James S. Evans
Alizee Zimmerman
Stacey M. Williams
Marilyn Brandt
Moriah Sevier
Samuel Gittens
Kayla A. Budd
Matthew Warham
William C. Sharp
Gabriel A. Delgado
Alwin Hylkema
Kimani Kitson-Walters
Jean-Pascal Quod
Mya Breitbart
Ian Hewson
author_sort Brayan Vilanova-Cuevas
collection DOAJ
description ABSTRACT Mass mortality of Diadematidae urchins, caused by the Diadema antillarum scuticociliatosis 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 abnormal Diadema antillarum were collected in the field during the initial assessment of the DSc causative agent and from an experimental challenge of DScPc culture on aquacultured D. 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, Kistimonas spp., Propionigenium spp., and Endozoicomonas spp. were highly represented in amplicon libraries. DSc-affected urchin amplicon libraries had lower taxonomic richness and a greater representation of taxa related to Fangia hongkongensis and Psychrobium spp. Amplicon libraries of urchins experimentally challenged with the DSc pathogen had some shifts in microbial composition, but F. hongkongensis was not a part of the core bacteria in DSc-challenged specimens. DSc-affected Echinothrix diadema from Réunion Island showed a similar high representation of F. hongkongensis as that seen on Caribbean D. antillarum. Our results suggest that DSc alters Diadematidae microbiomes and that F. hongkongensis may 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 to Diadema antillarum scuticociliatosis (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 of Fangia hongkongensis and Psychrobium spp. The findings indicate that F. hongkongensis could 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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spelling doaj-art-1809dd233ecf45b48d89f0fa6c4603be2025-08-20T02:56:27ZengAmerican Society for MicrobiologymSystems2379-50772025-03-0110310.1128/msystems.01418-24Investigating the influence of Diadematidae scuticociliatosis on host microbiome compositionBrayan Vilanova-Cuevas0Christopher M. DeRito1Isabella T. Ritchie2Christina A. Kellogg3James S. Evans4Alizee Zimmerman5Stacey M. Williams6Marilyn Brandt7Moriah Sevier8Samuel Gittens9Kayla A. Budd10Matthew Warham11William C. Sharp12Gabriel A. Delgado13Alwin Hylkema14Kimani Kitson-Walters15Jean-Pascal Quod16Mya Breitbart17Ian Hewson18Department of Microbiology, Cornell University, Ithaca, New York, USADepartment of Microbiology, Cornell University, Ithaca, New York, USACollege of Marine Science, University of South, St. Petersburg, Florida, USAU.S. Geological Survey St Petersburg Coastal and Marine Science Center, St. Petersburg, Florida, USAU.S. Geological Survey St Petersburg Coastal and Marine Science Center, St. Petersburg, Florida, USATurks and Caicos Reef Fund, Providenciales, Turks and Caicos IslandsInstitute for Socio-Ecological Research, Cabo Rojo, Puerto Rico, USACenter for Marine and Environmental Studies, University of the Virgin Islands, Saint Thomas, Virgin Islands, USACenter for Marine and Environmental Studies, University of the Virgin Islands, Saint Thomas, Virgin Islands, USACenter for Marine and Environmental Studies, University of the Virgin Islands, Saint Thomas, Virgin Islands, USACenter for Marine and Environmental Studies, University of the Virgin Islands, Saint Thomas, Virgin Islands, USADepartment of Planning and Natural Resources, Virgin Islands Government, Christiansted, Virgin Islands, USAFlorida Fish and Wildlife Conservation Commission, Fish and Wildlife Research Institute, Marathon, Florida, USAFlorida Fish and Wildlife Conservation Commission, Fish and Wildlife Research Institute, Marathon, Florida, USAVan Hall Larenstein University of Applied Sciences, Leeuwarden, NetherlandsCaribbean Netherlands Science Institute, St. Eustatius, Caribbean, NetherlandsARVAM, c/o association Technopole de la Réunion, Sainte Clotide, Réunion, FranceCollege of Marine Science, University of South, St. Petersburg, Florida, USADepartment of Microbiology, Cornell University, Ithaca, New York, USAABSTRACT Mass mortality of Diadematidae urchins, caused by the Diadema antillarum scuticociliatosis 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 abnormal Diadema antillarum were collected in the field during the initial assessment of the DSc causative agent and from an experimental challenge of DScPc culture on aquacultured D. 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, Kistimonas spp., Propionigenium spp., and Endozoicomonas spp. were highly represented in amplicon libraries. DSc-affected urchin amplicon libraries had lower taxonomic richness and a greater representation of taxa related to Fangia hongkongensis and Psychrobium spp. Amplicon libraries of urchins experimentally challenged with the DSc pathogen had some shifts in microbial composition, but F. hongkongensis was not a part of the core bacteria in DSc-challenged specimens. DSc-affected Echinothrix diadema from Réunion Island showed a similar high representation of F. hongkongensis as that seen on Caribbean D. antillarum. Our results suggest that DSc alters Diadematidae microbiomes and that F. hongkongensis may 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 to Diadema antillarum scuticociliatosis (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 of Fangia hongkongensis and Psychrobium spp. The findings indicate that F. hongkongensis could 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.https://journals.asm.org/doi/10.1128/msystems.01418-24microbiomediseaseDiadema antillarumscuticociliatosis
spellingShingle Brayan Vilanova-Cuevas
Christopher M. DeRito
Isabella T. Ritchie
Christina A. Kellogg
James S. Evans
Alizee Zimmerman
Stacey M. Williams
Marilyn Brandt
Moriah Sevier
Samuel Gittens
Kayla A. Budd
Matthew Warham
William C. Sharp
Gabriel A. Delgado
Alwin Hylkema
Kimani Kitson-Walters
Jean-Pascal Quod
Mya Breitbart
Ian Hewson
Investigating the influence of Diadematidae scuticociliatosis on host microbiome composition
mSystems
microbiome
disease
Diadema antillarum
scuticociliatosis
title Investigating the influence of Diadematidae scuticociliatosis on host microbiome composition
title_full Investigating the influence of Diadematidae scuticociliatosis on host microbiome composition
title_fullStr Investigating the influence of Diadematidae scuticociliatosis on host microbiome composition
title_full_unstemmed Investigating the influence of Diadematidae scuticociliatosis on host microbiome composition
title_short Investigating the influence of Diadematidae scuticociliatosis on host microbiome composition
title_sort investigating the influence of diadematidae scuticociliatosis on host microbiome composition
topic microbiome
disease
Diadema antillarum
scuticociliatosis
url https://journals.asm.org/doi/10.1128/msystems.01418-24
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