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Symbiodiniaceae diversity and characterization of palytoxin in various zoantharians (Anthozoa, Hexacorallia)

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Abstract

Anemone-like animals belonging to the order Zoantharia are common anthozoans widely distributed from shallow to deep tropical and subtropical waters. Some species are well-known because of their high toxicity due to the presence of palytoxin (PLTX) in their tissues. PLTX is a large polyhydroxylated compound and one of the most potent toxins known. Currently, the PLTX biosynthetic pathway in zoantharians and the role of the host or the putative symbiotic organism(s) involved in this pathway are entirely unknown. To better understand the presence of PLTX in some Zoantharia, twenty-nine zoantharian colonies were analysed in this study. All zoantharian samples and their endosymbiotic dinoflagellates (Symbiodiniaceae = Zooxanthellae) were identified using DNA barcoding and phylogenetic reconstructions. Quantification of PLTX and its analogues showed that the yields contained in Palythoa heliodiscus, Palythoa aff. clavata and one potentially undescribed species of Palythoa are among the highest ever found (up to > 2 mg/g of wet zoantharian). Mass spectrometry imaging was used for the first time on Palythoa samples and revealed that in situ distribution of PLTX is mainly located in ectodermal tissues such as the epidermis of the body wall and the pharynx. Moreover, high levels of PLTX have been detected in histological regions where few or no Symbiodiniaceae cells could be observed. Finally, issues such as host‐specificity and environmental variables driving biogeographical patterns of hosted Symbiodiniaceae in zoantharian lineages were discussed in light of our phylogenetic results as well as the patterns of PLTX distribution. It was concluded that (1) the variability of Symbiodiniaceae diversity may be related to ecological divergence in Zoantharia, (2) all Palythoa species hosted Cladocopium Symbiodiniaceae (formerly clade C), (3) the sole presence of Cladocopium is not sufficient to explain the presence of high concentrations of PLTX and/or its analogues, and (4) the ability to produce high levels of PLTX and/or its analogues highlighted in some Palythoa species could be a plesiomorphic character inherited from their last common ancestor and subsequently lost in several lineages.

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Data availability

All sequences generated in this study have been deposited and accepted in GenBank (MW077616 to MW077644, MW219226 to MW219250, MW717422 to MW717450). The datasets generated during and/or analysed during the current study are available from the corresponding author on reasonable request.

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Acknowledgements

We are deeply grateful to James Reimer for helpful discussions on the systematics and phylogeny of Zoantharia during this study. The authors also wish to thank Daniel Papillon who provided English corrections. Sampling of zoantharians by diving in the Caribbean was made possible by a commercial MLD collection license from the US Government (State of Florida SPL #932658 with MLD endorsement #1117).

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Author notes

  1. Jean Lorquin and Yvan Perez contributed equally to this work.

Authors and Affiliations

  1. Mediterranean Institute of Oceanography (MIO) UM 110, Aix-Marseille University, CNRS, University of Toulon, Marseille, IRD, France

    Ludovic Sawelew & Jean Lorquin

  2. Mediterranean Institute of Marine and Terrestrial Biodiversity and Ecology (IMBE) UMR 7263, Aix-Marseille University, University of Avignon, CNRS, Marseille, IRD, France

    Ludovic Sawelew & Yvan Perez

  3. Coral Biome SAS, Zone Luminy Entreprises, 163 avenue de Luminy, 13288 Marseille cedex 9, Marseille, France

    Ludovic Sawelew

  4. Membrane Transporters, Chemoresistance and Drug design UMR-MD1, Faculty Medical, Aix-Marseille University, Marseille, France

    Christopher Nuccio

  5. Coral Morphologic Aquaculture Research Lab, 800 NW 7th Avenue Miami, Miami, FL, 33136, USA

    Colin Foord

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  1. Ludovic Sawelew
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  3. Colin Foord
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  4. Jean Lorquin
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Contributions

LS and YP carried out the molecular experiments and phylogenetic analyses. LS and JL did the PLTX purification, HPLC, and mass spectrometry experiments. LS, CN, and JL did the MALDI-IMS analyses. CF collected specimens of Zoanthus and Palythoa species in Florida and maintained the clonal populations of Palythoa aff. clavata and P. heliodiscus. JL, YP, and LS drafted the manuscript. JL and YP conceived and supervised the study. All authors read, amended, and approved the final manuscript.

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Correspondence to Ludovic Sawelew.

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Sawelew, L., Nuccio, C., Foord, C. et al. Symbiodiniaceae diversity and characterization of palytoxin in various zoantharians (Anthozoa, Hexacorallia). Org Divers Evol 22, 555–576 (2022). https://doi.org/10.1007/s13127-022-00550-2

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