Systematics, Biodiversity and Evolution of Plants
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Wednesday June 8, 2022, 5pm CEST

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PHILIPP HESS1*, KENNETH MERTENS2, NICOLAS CHOMERAT2, VERONIQUE SECHET3, FABIENNE HERVE1, LOÏC PLESSIS1, DAMIEN REVEILLON1, PATRICE BREHMER

Vulcanodinium rugosum - a potent and ubiquitous genus affecting mice and man 

1 Ifremer, PHYTOX, Laboratoire METALG, 44000 Nantes, France
2 Ifremer, LITTORAL, LER-BO, 29000 Concarneau, France
3Ifremer, PHYTOX, Laboratoire PHYSALG, 4400, France
4 IRD, Univ Brest, CNRS, Ifremer, Lemar, Sub Regional Fisheries Commission (SRFC), Dakar, Senegal
* philipp.hess@ifremer.fr

 

The monotypic genus Vulcanodinium was erected in 2011 [1], and the unique species V. rugosum was associated with the production of pinnatoxins the same year [2]. According to its morphology, V. rugosum is closely related to peridinioid/scrippsielloid dinoflagellates, such as the genus Bysmatrum from which it can be distinguished mainly by the pattern of anterior intercalary plates. Based on LSU rDNA sequence data, the taxon was shown to belong to the order Peridiniales but it was not possible to affiliate it to a particular family, and molecular data showing a rather high divergence from other peridinioids supports the erection of the genus. Few studies focused on the life cycle of this organism [3, 4], but while V. rugosum has been observed as a pelagic species, it also frequently forms clusters of non-motile (temporary cyst-like) cells embedded in a highly adherent mucous. Its pelagic life forms obviously may contribute to its spread and some of the effects discussed below.
Pinnatoxins (PnTXs), and their derivatives, pteriatoxins (PtTXs), are a group of macrocycles with cyclic imine and spiro-functions similar to spirolides and have been identified in shellfish well before the discovery of their causative organism [5-9]. Pinnatoxins are potent neurotoxins that were discovered using an isolation scheme bioguided by intraperitoneal mouse bioassay [7]. The toxins act via blocking neurotransmission through their strong binding to the nicotinic acetylcholine receptor [10, 11], and also activate Ca2+-channels and inhibit expression of vascular cell adhesion molecule 1 (VCAM-1) [12]. After isolation of a peridinioid dinoflagellate producer in New Zealand and the isolation of pinnatoxins E and F in 2010 [13, 14], pinnatoxins were also rapidly reported in Australia, China, Japan, Canada and Europe in both algal strains and shellfish in areas of different ecology, notably Norway and France [2, 4, 15-20], even if numerous ecological studies suggest warm water temperatures as a driver for significant bloom development [21-24]. There is significant diversity of PnTXs among strains isolated from different regions which may vouch for further studies on intra-specific genetic diversity, and ballast water or other ship vectors have been suggested as a possible route of distribution of these organisms around the globe.
Studies on the cytotoxicity of the first French strain suggested presence of several toxins [25, 26]. Indeed, a novel toxin, i.e. portimine, was simultaneously reported from a New Zealand strain. Portimine is a small macrocycle that also contains a cyclic imine group but only a single carbon with spiro-functionality, and presents greater cytotoxicity than PnTXs. Contrarily to the diversity of PnTXs, all strains characterized globally appear to produce portimine. Shellfish appear to preferentially accumulate PnTXs rather than portimine, and PnTXs have been classified as fast acting or presenting atypical toxicity observed in mice, i.e. symptoms within 15 min. Still, to date, no acute intoxication through consumption of shellfish by humans has been confirmed to have been caused by PnTXs. Surprisingly, a bloom of V. rugosum in Cienfuegos Bay, Cuba, has been reported to cause dermatitis in bathers [24], and we report here an event in Senegal where, in addition to PnTX-H, record values for portimine occurred in an offshore environment affecting artisanal fishermen with similar symptoms in 2020 and 2021. Further research is underway to elucidate causative compounds and mechanisms of toxicity as well the genetic signature of strains involved.

References 

1. Nézan, E. and N. Chomérat, Vulcanodinium rugosum gen. et sp. nov. (Dinophyceae), un nouveau dinoflagellé marin de la côte méditerraneenne française. Cryptogamie, Algologie, 2011. 32(1): p. 3-18.
2. Rhodes, L., et al., Dinoflagellate Vulcanodinium rugosum identified as the causative organism of pinnatoxins in Australia, New Zealand and Japan. Phycologia, 2011. 50(6): p. 624-628.
3. Abadie, E., Etude de Vulcanodinium rugosum (Dinoflagellé producteur de pinnatoxines) se développant dans la lagune méditerranéenne de l’Ingril. 2015, Université de Montpellier.
4. Zeng, N., et al., The first report of Vulcanodinium rugosum (Dinophyceae) from the South China Sea with a focus on the life cycle. New Zealand Journal of Marine and Freshwater Research, 2012. 46(4): p. 511-521.
5. Zheng, S.Z., et al., The isolation and bioactivities of pinnatoxin. Chin. J. Mar. Drugs, 1990. 33: p. 33-35.
6. Chou, T., et al., Structure of pinnatoxins, potent shellfish poisons. Tennen Yuki Kagobutsu Toronkai Koen Yoshishu, 1994. 36th: p. 57-64.
7. Uemura, D., et al., Pinnatoxin A: a toxic amphoteric macroycle from the Okinawan bivalve Pinna muricata. J. Am. Chem. Soc., 1995. 117: p. 1155-1156.
8. Chou, T., et al., Isolation and structure of pinnatoxin D, a new shellfish poison from the okinawan bivalve Pinna muricata. Tetrahedron Letters, 1996. 37(23): p. 4027-4030.
9. Takada, N., et al., Structural determination of pteriatoxins A, B and C, extremely potent toxins from the bivalve Pteria penguin. Tetrahedron Letters, 2001. 42(20): p. 3495-3497.
10. Araoz, R., et al., Total Synthesis of Pinnatoxins A and G and Revision of the Mode of Action of Pinnatoxin A. Journal of the American Chemical Society, 2011. 133(27): p. 10499-10511.
11. Hellyer, S.D., et al., Marine algal pinnatoxins E and F cause neuromuscular block in an in vitro hemidiaphragm preparation. Toxicon, 2011. 58(8): p. 693-699.
12. Kuramoto, M., H. Arimoto, and D. Uemura, Studies in bioactive marine alkaloids. Journal of Synthetic Organic Chemistry Japan, 2003. 61(11): p. 1099-1105.
13. Rhodes, L., et al., Production of pinnatoxins by a peridinoid dinoflagellate isolated from Northland, New Zealand. Harmful Algae, 2010. 9(4): p. 384-389.
14. Selwood, A.I., et al., Isolation, Structural Determination and Acute Toxicity of Pinnatoxins E, F and G. Journal of Agricultural and Food Chemistry, 2010. 58(10): p. 6532-6542.
15. Rhodes, L., et al., Production of pinnatoxins E, F and G by scrippsielloid dinoflagellates isolated from Franklin Harbour, South Australia. New Zealand Journal of Marine and Freshwater Research, 2011. 45(4): p. 703-709.
16. Rundberget, T., et al., Pinnatoxins and spirolides in Norwegian blue mussels and seawater. Toxicon, 2011. 58(8): p. 700-11.
17. Smith, K.F., et al., A dinoflagellate producer of pinnatoxin G, isolated from sub-tropical Japanese waters. Harmful Algae, 2011. 10(6): p. 702-705.
18. Hess, P., et al., Pinnatoxines en lien avec l’espèce Vulcanodinium rugosum. 2012.
19. McCarron, P., et al., Identification of pinnatoxins and discovery of their fatty acid ester metabolites in mussels (Mytilus edulis) from Eastern Canada. Journal of Agricultural and Food Chemistry, 2012. 60(6): p. 1437-46.
20. Hess, P., et al., Pinnatoxin G is responsible for atypical toxicity in mussels (Mytilus galloprovincialis) and clams (Venerupis decussata) from Ingril, a French Mediterranean lagoon. Toxicon, 2013. 75: p. 16-26.
21. Hernandez-Becerril, D.U., M.C. Rodriguez-Palacio, and C. Lozano-Ramirez, Morphology and life stages of the potentially pinnatoxin-producing thecate dinoflagellate Vulcanodinium rugosum from the tropical Mexican Pacific. Botanica Marina, 2013. 56(5-6): p. 535-540.
22. Abadie, E., et al., Toxin and growth responses of the neurotoxic dinoflagellate Vulcanodinium rugosum to varying temperature and salinity. Toxins, 2016. 8(5): p. 18.
23. Abadie, E., et al., What are the main environmental factors driving the development of the neurotoxic dinoflagellate Vulcanodinium rugosum in a Mediterranean ecosystem (Ingril lagoon, France)? Harmful Algae, 2018. 75: p. 75-86.
24. Moreira-Gonzalez, A.R., et al., Summer bloom of Vulcanodinium rugosum in Cienfuegos Bay (Cuba) associated to dermatitis in swimmers. Science of the Total Environment, 2021. 757: p. 12.
25. Geiger, M., et al., Cytotoxicity, fractionation and dereplication of extracts of the dinoflagellate Vulcanodinium rugosum, a producer of Pinnatoxin G. Marine Drugs, 2013. 11(9): p. 3350-3371.
26. Geiger, M., et al., Cellular models and cytotoxicity of pinnatoxin-G and extracts of the dinoflagellate Vulcanodinium rugosum recently isolated from the French mediterranean lagoon of Ingril. Toxicon, 2013. 75(0): p. 215-216.