Ostreopsis cf. ovata and Ostreopsis lenticularis (DinophyceaeGonyaulacales) in the Galapagos Marine Reserve

  1. Carnicer, Olga 1
  2. Okolodkov, Yuri B. 2
  3. Garcia-Altares, María 3
  4. Keith, Inti 4
  5. Andree, Karl B. 5
  6. Diogène, Jorge 5
  7. Fernández-Tejedor, Margarita 5
  1. 1 Escuela de Gestión Ambiental, Pontificia Universidad Católica del Ecuador, Sede Esmeraldas (PUCESE)
  2. 2 Laboratorio de Botánica Marina y Planctología, Instituto de Ciencias Marinas y Pesquerías, Universidad Veracruzana (ICIMAP-UV)
  3. 3 Leibniz Institute for Natural Product Research and Infection Biology
  4. 4 Charles Darwin Research Station, Charles Darwin Foundation
  5. 5 Institut de Recerca i Tecnologia Agroalimentària (IRTA)
Revista:
Scientia Marina

ISSN: 0214-8358

Año de publicación: 2020

Volumen: 84

Número: 3

Páginas: 1-15

Tipo: Artículo

DOI: 10.3989/SCIMAR.05035.08A DIALNET GOOGLE SCHOLAR lock_openAcceso abierto editor

Otras publicaciones en: Scientia Marina

Resumen

El género de los dinoflagelados bentónicos Ostreopsis es de particular interés, porque algunas especies afectan negativamente a la salud humana y a los ecosistemas marinos costeros. Las poblaciones de Ostreopsis en áreas remotas, como la Reserva Marina de Galápagos con su biodiversidad única, pueden proporcionar datos significativos a su estudio. Se recolectaron muestras de dinoflagelados epibentónicos de dos islas (Santa Cruz y Santa Fé) en 2017. Se encontraron espe­cies de los géneros Gambierdiscus, Amphidinium, Coolia y Ostreopsis. Las cepas de Ostreopsis se aislaron para caracterizar su morfología, biología molecular y toxicidad. Se distinguieron tres morfotipos diferentes de Ostreopsis basados en tamaño (n=369). El morfotipo de células pequeñas fue dominante en diez muestras, con abundancias de hasta 33405 células g–1 de peso fresco de macroalgas. Se aisló un total de 16 cepas y se secuenciaron las regiones de rDNA, 5.8S y ITS para el estudio filogenético. Trece cepas pertenecieron al morfotipo de células pequeñas agrupadas en el clado O. cf. ovata Atlántico/Índio/Pacífico y tres cepas al morfotipo de células grandes agrupadas en el clado Ostreopsis lenticularis. Ninguna de las cepas aisladas resultó ser tóxica. La presencia de estos géneros/especies representa una amenaza potencial para los ecosistemas marinos, por lo que es importante tener en cuenta las especies bentónicas en la vigilancia de la proliferación de algas nocivas en la reserva.

Información de financiación

The authors would like to thank Josselyn B. Yépez Rendón (Esmeraldas, Ecuador) for her help in field work, Àngels Tudó (Institut de Recerca i Tecnologia Agroalimentària, IRTA, Sant Carles de la Ràpita, Spain) for her assistance in data analysis, and Marcia M. Gowing (University of California at Santa Cruz, California, USA) for improving the English style. The two anonymous reviewers are thanked for their valuable comments. This work was funded by the Pontifical Catholic University of Ecuador - Sede Esmeraldas through the internal project “Characterization of the epibenthic and phytoplanktonic microalgae community in the Galapagos Islands”. IK thanks Danny Rueda and the Galapagos National Park for granting us authorization to carry out this investigation (research permit number: PC-15–19). Additionally, IK would like to thank Galapagos Conservancy, Lindblad Expedition/ National Geographic Fund, Galapagos Conservation Trust, Paul M. Angell Foundation and Ecoventura for research funding provided for the CDF marine invasive species program. This publication is contribution number 2332 of the Charles Darwin Foundation for the Galapagos Islands.

Referencias bibliográficas

  • Accoroni S., Totti C. 2016. The toxic benthic dinoflagellates of the genus Ostreopsis in temperate areas: a review. Adv. Oceanogr. Limnol. 7: 1-15.
  • Accoroni S., Romagnoli T., Penna A., et al. 2016. Ostreopsis fattorussoi sp. nov. (Dinophyceae), a new benthic toxic Ostreopsis species from the eastern Mediterranean Sea. J. Phycol. 52: 1064-1084.
  • Aligizaki K., Nikolaidis G. 2006. The presence of the potentially toxic genera Ostreopsis and Coolia (Dinophyceae) in the North Aegean Sea, Greece. Harmful Algae 5: 717-730.
  • Andree K.B., Fernandez-Tejedor M., Elandaloussi L.M., et al. 2011. Quantitative PCR coupled with melt curve analysis for detection of selected Pseudo-nitzschia spp. (Bacillariophyceae) from the northwestern Mediterranean Sea. Appl. Environ. Microb. 77: 1651-1659.
  • Arbelaez N.M., Mancera Pineda J.E., Reguera B. 2017. Epiphytic dinoflagellates of Thalassia testudinum in two coastal systems of the Colombian Caribbean. Bol. Invest. Mar. Cost. - INVEMAR 46: 9-40.
  • Ashton M., Tosteson T., Tosteson C. 2003. The effect of elevated temperature on the toxicity of the laboratory cultured dinoflagellate Ostreopsis lenticularis (Dinophyceae). Rev. Biol. Trop. 51: 1-6.
  • Banks S. 2002. Ambiente físico. In: Danulat E., Edgar G.J. (eds), Reserva Marina de Galápagos. Línea base de la biodiversidad. Fundación Charles Darwin/Servicio Parque Nacional Galápagos, Santa Cruz, Galápagos, Ecuador, pp. 29-42.
  • Berdalet E., Tester P.A., Chinain M., et al. 2017. Harmful algal blooms in benthic systems: Recent progress and future research. Oceanography 30: 36-45.
  • Boisnoir A., Pascala P.Y., Cordonniera S., et al. 2019. Spatio-temporal dynamics and biotic substrate preferences of benthic dinoflagellates in the Lesser Antilles, Caribbean Sea. Harmful Algae 81: 18-29.
  • Carnicer O., Tunin-Ley A., Andree K.B., et al. 2015. Contribution to the genus Ostreopsis in Reunion Island (Indian Ocean): Molecular, morphologic and toxicity characterization. Cryptogamie Algol. 36: 101-119.
  • Carnicer O., García-Altares M., Andree K.B., et al. 2016a. First evidence of Ostreopsis cf. ovata in the eastern tropical Pacific Ocean, Ecuadorian coast. Bot. Mar. 59: 267-274.
  • Carnicer O., García-Altares M., Andree K.B., et al. 2016b. Ostreopsis cf. ovata from western Mediterranean Sea: Physiological responses under different temperature and salinity conditions. Harmful Algae 57: 98-108.
  • Carnicer O., De La Fuente P., Canepa A., et al. 2019. Marine dinoflagellate assemblage in the Galápagos Marine Reserve. Front. Mar. Sci. 6: 235.
  • Chang F.H., Shimizu Y., Hay B., et al. 2000. Three recently recorded Ostreopsis spp. (Dinophyceae) in New Zealand: Temporal and regional distribution in the upper North Island from 1995 to 1997. New Zeal. J. Mar. Fresh. Res. 34: 29-39.
  • Chomérat N., Bilien G., Derrien A., et al. 2019. Ostreopsis lenticularis Y. Fukuyo (Dinophyceae, Gonyaulacales) from French Polynesia (South Pacific Ocean): A revisit of its morphology, molecular phylogeny and toxicity. Harmful Algae 84: 95-111.
  • Chomérat N., Bilien G., Couté A., et al. 2020. Reinvestigation of Ostreopsis mascarenensis Quod (Dinophyceae, Gonyaulacales) from Reunion Island (SW Indian Ocean): molecular phylogeny and emended description. Phycologia 59: 140-153.
  • Ciminiello P., Dell’Aversano C., Dello Iacovo E., et al. 2011. LC-MS of palytoxin and its analogues: State of the art and future perspectives. Toxicon 57: 376-389.
  • Ciminiello P., Dell’Aversano C., Dello Iacovo E., et al. 2013. Investigation of toxin profile of Mediterranean and Atlantic strains of Ostreopsis cf. siamensis (Dinophyceae) by liquid chromatography-high resolution mass spectrometry. Harmful Algae 23: 19-27.
  • Ciminiello P., Dell’Aversano C., Dello Iacovo E., et al. 2015. Liquid chromatography-high-resolution mass spectrometry for palytoxins in mussels. Anal. Bioanal. Chem. 407: 1463-1473.
  • Cortés-Lara M.C., Cortés-Altamirano R., Sierra-Beltrán A., et al. 2005. Ostreopsis siamensis (Dinophyceae) a new tychoplanktonic record from Isabel Island National Park, Pacific Mexico. Harmful Algae News (IOC Newsletter on toxic algae and algal blooms) 28: 4-5.
  • David H., Laza-Martínez A., Miguel I., et al. 2013. Ostreopsis cf. siamensis and Ostreopsis cf. ovata from the Atlantic Iberian Peninsula: Morphological and phylogenetic characterization. Harmful Algae 30: 44-55.
  • Del Favero G., Sosa S., Pelin M., et al. 2012. Sanitary problems related to the presence of Ostreopsis spp. in the Mediterranean Sea: a multidisciplinary scientific approach. Annali dell’Istituto superiore di sanità48: 407-414.
  • Durán-Riveroll L.M., Cembella A.D., Okolodkov Y.B. 2019. A review on the biodiversity and biogeography of toxigenic benthic marine dinoflagellates of the coasts of Latin America. Front. Mar. Sci. 6: 148
  • Edgar G.J., Banks S.A., Brandt M., et al. 2010. El Niño, grazers and fisheries interact to greatly elevate extinction risk for Galapagos marine species. Global Change Biol. 16: 2876-2890.
  • Faust M.A. 1999. Three new Ostreopsis species (Dinophyceae): O. marinus sp. nov., O. belizeanus sp. nov., and O. caribeanus sp. nov. Phycologia 38: 92-99.
  • Faust M.A., Morton S.L. 1995. Morphology and ecology of the marine dinoflagellate Ostreopsis labens sp. nov. (Dinophyceae). J. Phycol. 31: 456-463.
  • Faust M.A., Morton S.L., Quod J.P. 1996. Further SEM study of marine dinoflagellates: the genus Ostreopsis (Dinophyceae). J. Phycol. 32: 1053-1065.
  • Fritz L., Triemer R.E. 1985. A rapid simple technique utilizing Calcofluor White M2R for the visualization of dinoflagellate thecal plates. J. Phycol. 21: 662-664.
  • Fukuyo Y. 1981. Taxonomical study on benthic dinoflagellates collected in coral reefs. Bull. Japan. Soc. Sci. Fish 47: 967-978.
  • Gárate-Lizárraga I., González-Armas R., Okolodkov Y.B. 2018. Occurrence of Ostreopsis lenticularis (Dinophyceae: Gonyaulacales) from the Archipiélago de Revillagigedo, Mexican Pacific. Mar. Pollut. Bull. 128: 390-395.
  • García-Altares M., Tartaglione L., Dell’Aversano C., et al. 2014. The novel OVTX-g and isobaric PLTX (so far referred to as putative PLTX) from Ostreopsis cf. ovata (NW Mediterranean Sea): structural insights by LC-high resolution MSn. Anal. Bioanal. Chem. 407: 1191-1204.
  • Guillard R.R.L. 1975. Culture of phytoplankton for feeding marine invertebrates. In: Smith W.L., Chanley M.H. (eds), Culture of marine invertebrate animals. Plenum Press, New York, pp. 29-60.
  • Hachani M.A., Dhib A., Fathallia A., et al. 2018. Harmful epiphytic dinoflagellate assemblages on macrophytes in the Gulf of Tunis. Harmful Algae 77: 29-42.
  • Hickman C.P.Jr. 2009. Evolutionary responses of marine invertebrates to insular isolation in Galapagos. Galapagos Res. 66: 32-42.
  • Holland W.C., Litaker R.W., Tomas C.R., et al. 2013. Differences in the toxicity of six Gambierdiscus (Dinophyceae) species measured using an in vitro human erythrocyte lysis assay. Toxicon. 65: 15-33.
  • Holmes M.K. 1998. Gambierdiscus yasumotoi sp. nov. (Dinophyceae), a toxic benthic dinoflagellate from southeastern Asia. J. Phycol. 34: 661-668.
  • Hoppenrath M., Murray S.A., Chomérat N., et al. 2014. Marine benthic dinoflagellates - unveiling their worldwide biodiversity. Schweizerbart’sche Verlagsbuchhandlung, Stuttgart, Germany, 276 pp.
  • Hoshaw R.W., Rosowski, J.R. 1973. Methods for microscopic algae. In: Stein J.R. (ed), Handbook of phycological methods: culture methods and growth measurements. Cambridge University Press, Cambridge, pp. 53-67.
  • Hwang B.S., Yoon E.Y., Kim H.S., et al. 2013. Ostreol A: a new cytotoxic compound isolated from the epiphytic dinoflagellate Ostreopsis cf. ovata from the coastal waters of Jeju Island, Korea. Bioorg, Med. Chem. Lett. 23: 3023-3027.
  • Irola-Sansores E.D., Delgado-Pech B., García-Mendoza E., et al. 2018. Population dynamics of benthic-epiphytic dinoflagellates on two macroalgae from coral reef systems of the northern Mexican Caribbean. Front. Mar. Sci. 5: 487.
  • John U., Litaker R.W., Montresor M., et al. 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.
  • Keith I., Dawson T.P., Collins K.J., et al. 2016. Marine invasive species: establishing pathways, their presence and potential threats in the Galapagos Marine Reserve. Pac. Conserv. Biol. 22: 377-385.
  • Kislik E., Saltos G., Torres G., et al. 2017. Biological hotspots in the Galápagos Islands: Exploring seasonal trends of ocean climate drivers to monitor algal blooms. Int. J. Bioeng. Life Sci. 11: 824-834.
  • Kumar S., Stecher G., Li M., et al. 2018. MEGA X: Molecular evolutionary genetics analysis across computing platforms. Mol. Biol. Evol. 35: 1547-1549.
  • Larsson M.E., Laczka O.F., Harwood D.T., et al. 2018. Toxicology of Gambierdiscus spp. (Dinophyceae) from tropical and temperate Australian waters. Mar. Drugs 16: 7.
  • Laza-Martínez A., Orive E., Miguel I. 2011. Morphological and genetic characterization of benthic dinoflagellates of the genera Coolia, Ostreopsis and Prorocentrum from the south-eastern Bay of Biscay. Eur. J. Phycol. 46: 45-65.
  • Laza-Martínez A., David H., Riobó P., et al. 2016. Characterization of a strain of Fukuyoa paulensis (Dinophyceae) from the western Mediterranean Sea. J. Eukaryot. Microbiol. 63: 481-497.
  • Leaw L.C., Teen L.P., Ahmad A., et al. 2001. Genetic diversity of Ostreopsis ovata (Dinophyceae) from Malaysia. Mar. Biotechnol. 3: 246-255.
  • Lenoir S., Ten-Hage L., Turquet J., et al. 2004. First evidence of palytoxin analogues from an Ostreopsis mascarenensis (Dinophyceae) benthic bloom in southwestern Indian Ocean. J. Phycol. 40: 1042-1051.
  • Litaker R.W., Vandersea M.W., Kibler S.R., et al. 2007. Recognizing dinoflagellate species using ITS rDNA sequences. J. Phycol. 43: 344-355.
  • Litaker R.W., Vandersea M.W., Faust M.A., et al. 2010. Global distribution of ciguatera causing dinoflagellates in the genus Gambierdiscus. Toxicon 56: 711-730.
  • Litaker R.W., Holland W.C., Hardison D.R., et al. 2017. Ciguatoxicity of Gambierdiscus and Fukuyoa species from the Caribbean and Gulf of Mexico. PLoS ONE 12: e0185776.
  • Liu Y., Xie L., Morrison J.M., et al. 2014. Ocean circulation and water mass characteristics around the Galápagos Archipelago simulated by a multiscale nested ocean circulation model. Int. J. Oceanogr. 2014: 198686.
  • Maciel-Baltazar E. 2015. Dinoflagelados (Dinoflagellata) tóxicos de la costa de Chiapas, México, Pacífico centro oriental. Cuad. Invest. UNED 7: 39-48.
  • Mendes M.C.Q., Nunes J.M.C., Menezes M., et al. 2017. Toxin production, growth kinetics and molecular characterization of Ostreopsis cf. ovata isolated from Todos os Santos Bay, tropical southwestern Atlantic. Toxicon 138: 18-30.
  • Menegotto A., Rangel T.F. 2018. Mapping knowledge gaps in marine diversity reveals a latitudinal gradient of missing species richness. Nat. Commun. 9: 4713.
  • Moreira A., Rodríguez F., Riobó P., et al. 2012. Notes on Ostreopsis sp. from southern-central coast of Cuba. Cryptogamie Algol. 33: 217-224.
  • Munday R., Murray S., Rhodes L.L., et al. 2017. Ciguatoxins and maitotoxins in extracts of sixteen Gambierdiscus isolates and one Fukuyoa isolate from the South Pacific and their toxicity to mice by intraperitoneal and oral administration. Mar. Drugs 15: 208.
  • Muromtsev A.M. 1963. The principal hydrology features of the Pacific Ocean. Jerusalem Post Press, Jerusalem, Israel, 417 pp.
  • Nascimento S.M., Correa E.V., Menezes M., et al. 2012. Growth and toxin profile of Ostreopsis cf. ovata (Dinophyta) from Rio de Janeiro, Brazil. Harmful Algae 13: 1-9.
  • Núñez-Vázquez E.J., Almazán-Becerril A., López-Cortés D.J., et al. 2019. Ciguatera in Mexico (1984-2013). Mar. Drugs 17: 13.
  • Penna A., Vila M., Fraga S., et al. 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., Fraga S., Battocchi C., et al. 2010. A phylogeographical study of the toxic benthic dinoflagellate genus Ostreopsis Schmidt. J. Biogeogr. 37: 830-841.
  • Penna A., Battocchi C., Capellacci S., et al. 2014. Mitochondrial, but not rDNA, genes fail to discriminate dinoflagellate species in the genus Ostreopsis. Harmful Algae 40: 40-50.
  • Quintana-Manotas H., Mercado-Gómez J. 2017. Composición de dinoflagelados epífitos y forófitos en la Costa norte del golfo de Morrosquillo, Sucre, Colombia. Rev. Colombiana Cienc. Anim. 9: 129-140.
  • Randall J.E. 2005. Review of clupeotoxism, an often fatal illness from the consumption of clupeoid fishes. Pac. Sci. 59: 73-77.
  • Rhodes L.L., Smith K.F., Verma A., et al. 2017. The dinoflagellate genera Gambierdiscus and Ostreopsis from subtropical Raoul Island and North Meyer Island, Kermadec Islands. New Zeal. J. Mar. Fresh. Res. 51: 490-504.
  • Riobó P., Paz B., Franco J.M., et al. 2008. Proposal for a simple and sensitive haemolytic assay for palytoxin: toxicological dynamics, kinetics, ouabain inhibition and thermal stability. Harmful Algae 7: 415-429.
  • Sato S., Nishimura T., Uehara K., et al. 2011. Phylogeography of Ostreopsis along west Pacific coast, with special reference to a novel clade from Japan. PloS ONE 6: e27983.
  • Schaeffer B.A., Morrison J.M., Kamykowski D., et al. 2008. Phytoplankton biomass distribution and identification of productive habitats within the Galápagos Marine Reserve by MODIS, a surface acquisition system, and in-situ measurements. Remote Sens. Environ. 112: 3044-3054.
  • Suzuki T., Watanabe R., Uchida H., et al. 2012. LC-MS/MS analysis of novel ovatoxin isomers in several Ostreopsis strains collected in Japan. Harmful Algae 20: 81-91.
  • Tamura K. 1992. Estimation of the number of nucleotide substitutions when there are strong transition-transversion and G + C-content biases. Mol. Biol. Evol. 9: 678-687.
  • Tartaglione L., Mazzeo A., Dell’Aversano C., et al. 2016. Chemical, molecular, and eco-toxicological investigation of Ostreopsis sp. from Cyprus Island: structural insights into four new ovatoxins by LC-HRMS/MS. Anal. Bioanal. Chem. 408: 915-932.
  • Tartaglione L., Dello Iacovo E., Mazzeo A., et al. 2017. Variability in toxin profiles of the Mediterranean Ostreopsis cf. ovata and in structural features of the produced ovatoxins. Environ. Sci. Technol. 51: 13920-13928.
  • Tawong W., Nishimura T., Sakanari H., et al. 2014. Distribution and molecular phylogeny of the dinoflagellate genus Ostreopsis in Thailand. Harmful Algae 37: 160-171.
  • Terajima T., Uchida H., Abe N., et al. 2018. Simple structural elucidation of ostreocin-B, a new palytoxin congener isolated from the marine dinoflagellate Ostreopsis siamensis, using complementary positive and negative ion liquid chromatography/quadrupole time-of-flight mass spectrometry. Rapid Commun. Mass Spectrom. 32: 1001-1007.
  • Tibiriçá C.E.J.A., Leite I.P., Batista T.V.V., et al. 2019. Ostreopsis cf. ovata bloom in Currais, Brazil: Phylogeny, toxin profile and contamination of mussels and marine plastic litter. Toxins 11: 446.
  • Tichadou L., Glaizal M., Armengaud A., et al. 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.
  • Torres G., Andrade C. 2014. Dinámica del plancton marino costero con relación al flujo de mareas en Bahía Aeolián en septiembre 2006 (Baltra-Galápagos-Ecuador). OceanDocs: Repository of Ocean Publications.
  • Uchida H., Taira Y., Yasumoto T. 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.
  • Vargas-Montero M., Morales A., Cortés J. 2012. Primer informe del género Gambierdiscus (Dinophyceae) y otros dinoflagelados bentónicos en el Parque Nacional Isla del Coco, Costa Rica, Pacífico Tropical Oriental. Rev. Biol. Trop. 60 (Suppl. 3): 187-199.
  • Verma A., Hoppenrath M., Harwood T., et al. 2016. Molecular phylogeny, morphology and toxigenicity of Ostreopsis cf. siamensis (Dinophyceae) from temperate south-east Australia. Phycol. Res. 64: 146-159.
  • Vila M., Abós-Herràndiz R., Isern-Fontanet J., et al. 2016. Establishing the link between Ostreopsis cf. ovata blooms and human health impacts using ecology and epidemiology. Sci. Mar. 80: 107-115.
  • Yépez Rendón J.B., Keith I., Ramírez Sarmiento A.K., et al. 2018. Presencia de microalgas epibentónicas en el Pacífico Este Tropical. Hallazgos 21 (Supl. especial): 1-23.
  • Zhang H., Lu S., Li Y., et al. 2018. Morphology and molecular phylogeny of Ostreopsis cf. ovata and O. lenticularis (Dinophyceae) from Hainan Island, South China Sea. Phycol. Res. 66: 3-14.