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Marine Natural Products from Zoantharians: Bioactivity, Biosynthesis, Systematics, and Cite This: DOI: 10.1039/C9np00043g Ecological Roles

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Marine Natural Products from Zoantharians: Bioactivity, Biosynthesis, Systematics, and Cite This: DOI: 10.1039/C9np00043g Ecological Roles Natural Product Reports View Article Online REVIEW View Journal Marine natural products from zoantharians: bioactivity, biosynthesis, systematics, and Cite this: DOI: 10.1039/c9np00043g ecological roles ab bc d Paul O. Guillen, † Karla B. Jaramillo, † Gregory´ Genta-Jouve and Olivier P. Thomas *a Covering: up to the end of 2018 Zoantharians, also improperly known as zoanthids or colonial anemones, are well known by aquarists because of their ease of use in aquaria but also because of their splendid colours. However, high concentrations of the highly toxic palytoxin found in some species of zoantharians maintained in reef aquaria has raised some issues recently, unveiling at the same time a rather unknown chemical diversity hidden in these marine beauties. Herein, we report the structure of the metabolites described in all species of zoantharians up to the end of 2018 and their associated biological activities. As sessile invertebrates, zoantharians harbour a rich diversity of micro-organisms that can play a role in the biosynthesis of these natural products and we detail the current hypotheses on the metabolic pathways leading to the identified ecdysteroids, zoanthoxanthins, zoanthamines, palytoxins and others. Finally, Received 13th July 2019 we assess the possible use of these metabolites in the systematics of such a complex group of marine DOI: 10.1039/c9np00043g invertebrates and we discuss their possible ecological roles. Altogether, this review brings some insights into rsc.li/npr the rich chemical diversity of zoantharians and their potential for marine biodiscovery and marine ecology. 1 Introduction 2.1.6.1 Palythoa 2 Chemical diversity and bioactivities 2.1.6.2 Zoanthus 2.1 Suborder Brachycnemina 2.2 The suborder Macrocnemina Published on 31 October 2019. Downloaded by NUI Galway 10/31/2019 11:35:38 AM. 2.1.1 Sterols 2.2.1 Ecdysteroids 2.1.1.1 Palythoa 2.2.1.1 Parazoanthus 2.1.1.2 Zoanthus 2.2.1.2 Savalia 2.1.2 Palytoxins 2.2.1.3 Antipathozoanthus 2.1.3 Ecdysteroids 2.2.2 2-Aminoimidazole alkaloids 2.1.3.1 Palythoa 2.2.2.1 Parazoanthus 2.1.4 Zoanthamine alkaloids 2.2.2.2 Epizoanthus 2.1.5 2-Aminoimidazole alkaloids 2.2.2.3 Terrazoanthus 2.1.5.1 Palythoa 2.2.3 Halogenated tyrosine derivatives 2.1.5.2 Zoanthus 2.2.3.1 Parazoanthus 2.1.6 Miscellaneous 2.2.3.2 Antipathozoanthus 3 Biosynthetic considerations 3.1 Ecdysteroids aMarine Biodiscovery, School of Chemistry and Ryan Institute, National University of Ireland Galway (NUI Galway), University Road, H91 TK33 Galway, Ireland. E-mail: 3.2 2-Aminoimidazole alkaloids [email protected] 3.3 Zoanthamines bESPOL Escuela Superior Polit´ecnica del Litoral, ESPOL, Centro Nacional de 3.4 Palytoxins Acuacultura e Investigaciones Marinas, Campus Gustavo Galindo km. 30.5 v´ıa 4 Systematics and ecological roles Perimetral, P. O. Box 09-01-5863, Guayaquil, Ecuador 4.1 Chemotaxonomic markers cZoology, School of Natural Sciences and Ryan Institute, National University of Ireland 4.1.1 Order Zoantharia Galway (NUI Galway), University Road, H91 TK33 Galway, Ireland dMus´eum National d'Histoire Naturelle, Unit´eMol´ecules de Communication et 4.1.1.1 Ecdysteroids Adaptation des Micro-organismes (UMR 7245), Sorbonne Universit´es, CNRS, Paris, 4.1.1.2 2-Aminoimidazole alkaloids France 4.1.2 Suborder Brachycnemina † Both authors contributed equally to this work. This journal is © The Royal Society of Chemistry 2019 Nat. Prod. Rep. View Article Online Natural Product Reports Review 4.1.2.1 Sterols 5 Conclusion 4.1.2.2 Zoanthamines 6 Conicts of interest 4.1.2.3 Palytoxins 7 Acknowledgements 4.1.3 Suborder Macrocnemina 8 Notes and references 4.1.3.1 2-Aminoimidazole alkaloids 4.1.3.2 Halogenated tyrosine derivatives 1 Introduction 4.2 Ecological roles 4.2.1 Ecdysteroids Long before the scientic explorations of our oceans and the 4.2.2 2-Aminoimidazole alkaloids advent of technological instruments such as SCUBA diving, 4.2.3 Suborder Brachycnemina people living in coastal regions had developed an acute sense of 4.2.3.1 Palytoxin observation that oen led to the creation of local myths. In 4.2.3.2 Zoanthamine remote islands of the Pacic, such as the island of Maui, 4.2.4 Suborder Macrocnemina Hawaii, an old legend described a green moss as “Limu Make O 4.2.4.1 Parazoanthus Hana” or the “Seaweed of Death from Hana”.1 The species, later Paul O. Guillen was born in Gr´egory Genta-Jouve is an asso- 1982. He obtained his BSc in ciate professor of natural prod- Pharmaceutical Biochemistry ucts chemistry at the University from the University of Cuenca Paris Descartes in France. In (Ecuador) followed by a MSc in 2011, he completed his PhD in Biotechnology from the Univer- Marine Natural Products sity of Melbourne (Australia), Chemistry at the University of which was supported by a schol- Nice Sophia Antipolis under the arship from the Ecuadorian supervision of Prof. Olivier P. government (SENESCYT). He is Thomas. Following a post- currently a PhD student in doctoral fellowship in Mark Chemistry at the National Viant's group at the University of University of Ireland Galway Birmingham (U.K.), he joined under the supervision of Prof. Olivier P. Thomas and Dr Jenny the University Paris Descartes (France) as a lecturer in 2013. His Rodriguez from the Centro Nacional de Acuicultura e Inves- main research interest lies in natural products anticipation using tigaciones Marinas (CENAIM-ESPOL, Ecuador). His research computational methods. Aer a period as visiting associate activities are focused on the natural product chemistry of zoan- professor at the National Museum of Natural History of Paris tharians present in the Tropical Eastern Pacic. (France), he is currently a visiting researcher at USR CNRS LEEISA Published on 31 October 2019. Downloaded by NUI Galway 10/31/2019 11:35:38 AM. in French Guiana. Karla B. Jaramillo was born in Olivier P. Thomas is an estab- 1988 and obtained her BSc lished professor in Marine Bio- degree in Marine Biology from discovery at the National the State University of Santa University of Ireland Galway Elena Peninsula (Ecuador). (NUIG). In 2002, he obtained his Currently, she is a PhD student PhD degree in Medicinal Chem- in Zoology at the National istry from the University of Paris University of Ireland Galway Descartes (France), followed by under the supervision of Prof. 2 years postdoctoral research at Grace McCormack and Prof. the French Atomic Energy Olivier P. Thomas. In 2016, she Commission, Saclay, working on received a visiting research grant the biochemistry of proteins. He to be trained on the taxonomy of was then recruited by the zoantharians at the University of the Ryukyus (Japan) under the University of Nice Sophia Antipolis (France) as a lecturer and was supervision of Dr Fr´ed´eric Sinniger. Her research work, also sup- promoted to a full professor in marine natural products in 2012. ported by CENAIM-ESPOL (Ecuador), is about the integrative Since 2015, he has been coordinating the Marine Biodiscovery taxonomy of zoantharians and octocorals using metabolomic group at NUIG, whose research activities are centred on the approaches as a complementary tool for the systematics of these natural products present in marine invertebrates but also in organisms. microalgae, their biosynthesis, ecological roles and also their applications in different sectors, like the pharmaceutical industry. Nat. Prod. Rep. This journal is © The Royal Society of Chemistry 2019 View Article Online Review Natural Product Reports identied as the zoantharian Palythoa toxica, was indeed found Marshall Islands by gas liquid chromatography. Palythoa to bioaccumulate one of the most complex and potent toxins tuberculosa showed a sterol composition similar to the previ- called palytoxin.2 Today, the use of tropical species of zoan- ously reported palysterol of P. mammilosa.5 The sterols from P. tharians in reef aquaria is mainly a consequence of the fasci- tuberculosa were identied as cholesterol (1), brassicasterol nating colours exhibited by these organisms. However, the (2), 22,23-dihydrobrassicasterol (3), gorgosterol (4), campes- presence of toxins has become a health concern for aquarists terol (5)andb-sitosterol (6)(Fig.1).Chalinasterol(7)wasre- and a better knowledge of their chemical diversity is needed. ported as the unique sterol from the Tahitian Palythoa sp. The Despite the occurrence of bioactive metabolites in relatively identication of the sterols was deduced from a comparison of common sessile invertebrates of the order Zoantharia, before theIRandNMRdatawiththoseof acetate derivatives and called Zoanthidea (Cnidaria: Anthozoa: Hexacorallia), this standards. Quinn et al. analysed the sterol composition of group has largely been overlooked in marine biodiscovery eight Hawaiian zoantharians, including four species of Paly- studies mostly focused on sponges or ascidians. Species of this thoa, as a preliminary taxonomic assessment.6 Methyl- order are nevertheless largely distributed in all the oceans, and enecholesterol (7), also named chalinasterol, was the only they have been described inhabiting very shallow or even sterol found in P. toxica,likeinPalythoa sp. from Tahiti re- intertidal waters until the deep-sea with a large proportion ported by Gupta and Scheuer.5 The sterol mixture of P. tuber- living in close association with cnidarians or sponges. Zoan- culosa, P. psammophilia and P. vestitus (previously known as tharians are anthozoan as characterized by an absence of a solid Zoanthus vestitus) showed a similar composition. The analysis skeleton and their ability of incorporating particles of sand or of the sterols of a Palythoa sp. collected in Okinawa, Japan, other material. A search of the natural products classied in the revealed the presence of cholesta-5,22(E)-dien-3b-ol (8), along order Zoantharia in the database Marinlit only retrieved 55 with 1, 2, 3, 4, 7, and traces of 23,24-dimethylcholesta-5,22(E)- metabolites, excluding the rst metabolites isolated due to dien-3b-ol (9)(Fig.1).7 The sterol 9, commonly found in unproper taxonomic description.3 We therefore believed that octocorals, is considered an intermediate in the biosynthesis a comprehensive inventory of the metabolites isolated from the of gorgosterol (4).
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