First evidence of <i>Ostreopsis</i> cf. <i>ovata</i> in the eastern tropical Pacific Ocean, Ecuadorian coast

  1. Carnicer, Olga 1
  2. García-Altares, María 2
  3. Andree, Karl B. 3
  4. Diogène, Jorge 3
  5. Fernández-Tejedor, Margarita 3
  1. 1 Universidad Politécnica de Cartagena
    info

    Universidad Politécnica de Cartagena

    Cartagena, España

    ROR https://ror.org/02k5kx966

  2. 2 Leibniz Institute for Natural Product Research and Infection Biology, Adolf-Reichwein-Straße 23, 07745 Jena, Germany
  3. 3 Institut de Recerca i Tecnologia Agroalimentària, IRTA, Carretera de Poble Nou, km 5.5, 43540 Sant Carles de la Ràpita, Spain
Revista:
Botanica Marina

ISSN: 1437-4323 0006-8055

Año de publicación: 2016

Volumen: 59

Número: 4

Páginas: 267-274

Tipo: Artículo

DOI: 10.1515/BOT-2016-0022 GOOGLE SCHOLAR

Otras publicaciones en: Botanica Marina

Objetivos de desarrollo sostenible

Resumen

Ostreopsis cf. ovata has become one of the most studied toxic dinoflagellates in the last decade due to the production of palytoxin-like analogues by some of the strains. Nonetheless, its taxonomy is still unresolved, as the morphological features are not well defined. Currently, three genetic clades of O. cf. ovata occurring in overlapping geographical areas, and several different toxicity patterns have been described. In this investigation, 13 isolates from the coast of Ecuador in the eastern Pacific Ocean, including a geographical area from which no information existed, were analyzed for Ostreopsis genotypes and toxicity of the O. cf. ovata complex. By analyzing the ITS and 5.8S rDNA, the isolates were found to be identical and to cluster in the Atlantic/Indian/Pacific clade, and they were not toxic according to hemolytic assays. The absence of palytoxin-like compounds was confirmed by liquid chromatography-mass spectrometry. The results are discussed in light of the current situation of O. cf. ovata strains, whose study has been traditionally restricted to some areas such as the Mediterranean Sea and the western Pacific Ocean. We also review the information regarding toxicity and molecular biology of O. cf. ovata strains in order to contribute to current understanding of the species complex.

Referencias bibliográficas

  • Accoroni, S., T. Romagnoli, F. Colombo, C. Pennesi, C.G. Di Camillo, M. Marini, C. Battocchi, P. Ciminiello, C. Dell’Aversano, E. Dello Iacovo, E. Fattorusso, L. Tartaglione, A. Penna and C. Totti. 2011. Ostreopsis cf. ovata bloom in the northern Adriatic Sea during summer 2009: ecology, molecular characterization and toxin profile. Mar. Pollut. Bull.62: 2512–2519.
  • Anderson, D.M., T.J. Alpermann, A.D. Cembella, Y. Collos, E. Masseret and M. Montresor. 2012. The globally distributed genus Alexandrium: Multifaceted roles in marine ecosystems and impacts on human health. Harmful Algae14: 10–35.
  • Andree, K.B., M. Fernández-Tejedor, L.M. Elandaloussi, S. Quijano-Scheggia, N. Sampedro, E. Garcés and J. Diogène. 2011. Quantitative PCR coupled with melt curve analysis for detection of selected Pseudo-nitzschia spp. (Bacillariophyceae) from the northwestern Mediterranean Sea. Appl. Environ. Microbiol.77: 1651–1659.
  • Biré, R., S. Trotereau, R. Lemée, D. Oregioni, C. Delpont, S. Krys and T. Guérin. 2015. Hunt for palytoxins in a wide variety of marine organisms harvested in 2010 on the French Mediterranean Coast. Marine Drugs13: 5425–5446.
  • Brissard, C., F. Hervé, M. Sibat, V. Sechet, P. Hess, Z. Amzil and C. Herrenknecht. 2014. Characterization of ovatoxin-h, a new ovatoxin analog, and evaluation of chromatographic columns for ovatoxin analysis and purification. J. Chromatogr. A.1388: 87–101.
  • Carnicer, O., C. Guallar, K.B. Andree, J. Diogène and M. Fernández-Tejedor. 2015a. Ostreopsis cf. ovata dynamics in the NW Medierranean Sea in relation to biotic and abiotic factors. Environ. Res.143: 89–99.
  • Carnicer, O., A. Tunin-Ley, K.B. Andree, J. Turquet, J. Diogène and M. Fernández-Tejedor. 2015b. Contribution to the genus Ostreopsis in Reunion Island (Indian Ocean): molecular, morphologic and toxicity characterization. Cryptogamie Algol. 36: 101–119.
  • Ciminiello, P., C. Dell’Aversano, E. Dello Iacovo, E. Fatturosso, M. Forino, L. Grauso, L. Targlione, F. Guerrini and R. Pistocchi. 2010. Complex palytoxin-like profile of Ostreopsis ovata. Identification of four new ovatoxins by high-resolution liquid chromatography/mass spectrometry. Rapid Commun. Mass Spectrom.24: 2735–2744.
  • Ciminiello, P., C. Dell’Aversano, E. Dello Iacovo, E. Fattorusso, M. Forino and L. Tartaglione. 2011. LC-MS of palytoxin and its analogues: state of the art and future perspectives. Toxicon57: 376–389.
  • Ciminiello, P., C.D. Aversano, E. Dello Iacovo, E. Fattorusso, M. Forino, L. Tartaglione and A. Penna. 2012. Unique toxin profile of a Mediterranean Ostreopsis cf. ovata strain: HR LC-MS, characterization of ovatoxin-f, a new palytoxin congener. Chem. Res. Toxicol.25: 1243–1252.
  • Ciminiello, P., C. Dell’Aversano, E. Dello Iacovo, M. Forino and L. Tartaglione. 2015. Liquid chromatography-high-resolution mass spectrometry for palytoxins in mussels. Anal. Bioanal. Chem.407: 1463–1473.
  • David, H., A. Laza-Martínez, I. Miguel and E. Orive. 2013. Ostreopsis cf. siamensis and Ostreopsis cf. ovata from the Atlantic Iberian Peninsula: morphological and phylogenetic characterization. Harmful Algae30: 44–55.
  • Faust, M.A., S.L. Morton and J.P. Quod. 1996. Further SEM study of marine dinoflagellates: the genus Ostreopsis (Dinophyceae) in the Atlantic cost of the Iberian Peninsula and sea-surface temperature. J. Phycol. 31: 456–463.
  • García-Altares, M., L. Tartaglione, C. Dell’Aversano, O. Carnicer, P. de la Iglesia, M. Forino, J. Diogène and P. Ciminiello. 2015. The novel ovatoxin-g and isobaric palytoxin (so far referred to as putative palytoxin) from Ostreopsis cf. ovata (NW Mediterranean Sea): structural insights by LC-high resolution MSn. Anal. Bioanal. Chem. 407: 1191–1204.
  • Hall, T.A. 1999. BioEdit, a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp. Ser. 41: 95–98.
  • Hallegraeff, G.M. 1998. Transport of toxic dinoflagellates via ships’ ballast water: Bioeconomic risk assessment and efficacy of possible ballast water management strategies. Mar. Ecol. Prog. Ser.168: 297–309.
  • Hwang, B.S., E.Y. Yoon, H.S. Kim, W. Yih, J.Y. Park, H.J. Jeong and J.-R. Rho. 2013. Ostreol A: a new cytotoxic compound isolated from the epiphytic dinollagellate Ostreopsis cf. ovata from the coastal waters of Jeju Island, Korea. Bioorg. Med. Chem. Lett. 23: 3023–3027.
  • John, U., R.W. Litaker, M. Montresor, S. Murray, M.L. Brosnahan and D.M. Anderson. 2014. Formal revision of the Alexandrium tamarense species complex (Dinophyceae) taxonomy: the introduction of five species with emphasis on molecular-based (rDNA) classification. Protist, 165: 779–804.
  • Kang, N.S., H.J. Jeong, S.Y. Lee, A.S. Lim, M.J. Lee, H.S. Kim and W. Yih. 2013. Morphology and molecular characterization of the epiphytic benthic dinoflagellate Ostreopsis cf. ovata in the temperate waters off Jeju Island, Korea. Harmful Algae27: 98–112.
  • Kimura, M. 1980. A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J. Mol. Evol. 16: 111–120.
  • Litaker, W.R., M.W. Vandersea, S.R. Kibler, K.S. Reece, N.A. Stokes, F.M. Lutzoni, B A. Yonish, M.A. West, M.N.D. Black and P.A. Tester. 2007. Recognizing dinoflagellate species using ITS rDNA sequences. J. Phycol.43: 344–355.
  • Mangialajo, L., R. Bertolotto, R. Cattaneo-Vietti, M. Chiantore, C. Grillo, R. Lemee, N. Melchiorre, P. Moretto, P. Povero and N. Ruggieri. 2011. Trends in Ostreopsis proliferation along the Northern Mediterranean coasts. Toxicon57: 408–420.
  • Nascimento, S.M., E.V. Corrêa, M. Menezes, D. Varela, J. Paredes and S. Morris. 2012. Growth and toxin profile of Ostreopsis cf. ovata (Dinophyta) from Rio de Janeiro, Brazil. Harmful Algae13: 1–9.
  • Okolodkov, Y.B. and I. Garate-Lizárraga. 2006. An annotated checklist of dinoflagellates (Dinophyceae) from Mexican Pacific. Acta Bot. Mar.154: 1–154.
  • Parsons, M.L., K. Aligizaki, M.-Y.D. Bottein, S. Fraga, S.L. Morton, A. Penna and L. Rhodes. 2012. Gambierdiscus and Ostreopsis: Reassessment of the state of knowledge of their taxonomy, geography, ecophysiology, and toxicology. Harmful Algae14: 107–129.
  • Pelin, M., M. Forino, V. Brovedani, L. Tartaglione, C. Dell’Aversano, R. Pistocchi, M. Poli, S. Sosa, C. Florio, P. Ciminiello and A. Tubaro. 2016. Ovatoxin-a, a palytoxin analogue isolated from Ostreopsis cf. ovata Fukuyo: cytotoxic activity and ELISA detection. Environ. Sci. Technol. 50: 1544–1551.
  • Penna, A., M. Vila, S. Fraga, M.G. Giacobbe, F. Andreoni, P. Riobó and C. Vernesi. 2005. Characterization of Ostreopsis and Coolia (Dinophyceae) isolates in the western Mediterranean Sea based on morphology, toxicity and internal transcribed spacer 5.8S rDNA sequences. J. Phycol.41: 212–225.
  • Penna, A., S. Fraga, C. Battocchi, S. Casabianca, M.G. Giacobbe, P. Riobó and C. Vernesi. 2010. A phylogeographical study of the toxic benthic dinoflagellate genus Ostreopsis Schmidt. J. Biogeogr. 37: 830–841.
  • Penna, A., C. Battocchi, S. Capellacci, S. Fraga, K. Aligizaki, R. Lemée and C. Vernesi. 2014. Mitochondrial, but not rDNA, genes fail to discriminate dinoflagellate species in the genus Ostreopsis. Harmful Algae40: 40–50.
  • Pezzolesi, L., F. Guerrini, P. Ciminiello, C. Dell’Aversano, E. Dello Iacovo, E. Fattorusso, M. Forino, L. Tartaglione and R. Pistocchi. 2012. Influence of temperature and salinity on Ostreopsis cf. ovata growth and evaluation of toxin content through HR LC-MS and biological assays. Water Research46: 82–92.
  • Pin, L.C., L.P. Teen, A. Ahmad and G. Usup. 2001. Genetic diversity of Ostreopsis ovata (Dinophyceae) from Malaysia. Marine Biotechnol.3: 246–255.
  • Rhodes, L. 2011. World-wide occurrence of the toxic dinoflagellate genus Ostreopsis Schmidt. Toxicon57: 400–407.
  • Riobó, P., B. Paz, J.M. Franco, J.A. Vázquez and M.A. Murado. 2008. Proposal for a simple and sensitive haemolytic assay for palytoxin Toxicological dynamics, kinetics, ouabain inhibition and thermal stability. Harmful Algae7: 415–429.
  • Sato, S., T. Nishimura, K. Uehara, H. Sakanari, W. Tawong, N. Hariganeya, K. Smith, L. Rhodes, T. Yasumoto, Y. Taira, S. Suda, H. Yamaguchi and M. Adachi. 2011. Phylogeography of Ostreopsis along west Pacific coast, with special reference to a novel clade from Japan. PLoS One6: e27983.
  • Scalco, E., C. Brunet, F. Marino, R. Rossi, V. Soprano, A. Zingone and M. Montresor. 2012. Growth and toxicity responses of Mediterranean Ostreopsis cf. ovata to seasonal irradiance and temperature conditions. Harmful Algae17: 25–34.
  • Smayda, T.J. 2007. Reflections on the ballast water dispersal harmful algal bloom paradigm. Harmful Algae6: 601–622.
  • Suzuki, T., R. Watanabe, H. Uchida, R. Matsushima, H. Nagai, T. Yasumoto, T. Yoshimatsu, S. Sato and M. Adachi. 2012. LC-MS/MS analysis of novel ovatoxin isomers in several Ostreopsis strains collected in Japan. Harmful Algae 20: 81–91.
  • Tartaglione, L., A. Mazzeo, C. Dell’Aversano, M. Forino, V. Giussani, S. Capellacci, A. Penna, V. Asnaghi, M. Faimali, M. Chiantore, T. Yasumoto and P. Ciminiello. 2016. Chemical, molecular, and eco-toxicological investigation of Ostreopsis sp. from Cyprius Island: structural insights into four ovatoxins by LC-HRMS/MS. Anal. Bioanal. Chem.408: 915–932.
  • Tawong, W., T. Yoshimatsu, H. Yamaguichi and M. Adachi. 2015. Effects of temperature, salinity and their interaction on growth of benthic dinoflagellates Ostreopsis spp. from Thailand. Harmful Algae 44: 37–45.
  • Tichadou, L., M. Glaizal, A. Armengaud, H. Grossel, R. Lemée, R. Kantin, J.L. Lasalle, G. Drouet, L. Rambaud, P. Malfait and L. de Haro. 2010. Health impact of unicellular algae of the Ostreopsis genus blooms in the Mediterranean Sea: experience of the French Mediterranean coast surveillance network from 2006 to 2009. Clin. Toxicol.48: 839–844.
  • Uchida, H., Y. Taira and T. Yasumoto. 2013. Structural elucidation of palytoxin analogs produced by the dinoflagellate Ostreopsis ovata IK2 strain by complementary use of positive and negative ion liquid chromatography/quadrupole time-of-flight mass spectrometry. Rapid Commun. Mass Spectrom.27: 1999–2008.
  • Vanucci, S., F. Guerrini, L. Pezzolesi, C. Dell’Aversano, P. Ciminiello and R. Pistocchi. 2012. Cell growth and toxins’ content of Ostreopsis cf. ovata in presence and absence of associated bacteria. Cryptogamie Algol.33: 105–112.