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

  1. García-Altares, María
  2. Tartaglione, Luciana
  3. Dell’Aversano, Carmela
  4. Carnicer, Olga 1
  5. de la Iglesia, Pablo
  6. Forino, Martino
  7. Diogène, Jorge
  8. Ciminiello, Patrizia
  1. 1 Universidad Politécnica de Cartagena
    info

    Universidad Politécnica de Cartagena

    Cartagena, España

    ROR https://ror.org/02k5kx966

Revista:
Analytical and Bioanalytical Chemistry

ISSN: 1618-2642 1618-2650

Año de publicación: 2014

Volumen: 407

Número: 4

Páginas: 1191-1204

Tipo: Artículo

DOI: 10.1007/S00216-014-8338-Y GOOGLE SCHOLAR lock_openAcceso abierto editor

Otras publicaciones en: Analytical and Bioanalytical Chemistry

Objetivos de desarrollo sostenible

Resumen

Blooms of the benthic dinoflagellate Ostreopsis cf. ovata are a concern in the Mediterranean Sea, since this species produces a wide range of palytoxin-like compounds listed among the most potent marine toxins. This study focused on two analogs of palytoxin found in cultures of six strains of O. cf. ovata isolated from the south of Catalonia (NW Mediterranean Sea). In addition to some already known ovatoxins, our strains produced two minor compounds, ovatoxin-g and the so far called putative palytoxin, whose structures had not been elucidated before. Insufficient quantity of these compounds impeded a full nuclear magnetic resonance (NMR)-based structural elucidation; thus, we studied their structure in crude algal extracts through liquid chromatography-electrospray ionization high-resolution mass spectrometry(n) (LC-ESI-HRMS(n)) in positive ion mode. Under the used MS conditions, the molecules underwent fragmentation at many sites of their backbone and a large number of diagnostic fragment ions were identified. As a result, tentative structures were assigned to both ovatoxin-g and the putative palytoxin, the latter being identified as a palytoxin isomer and re-named as isobaric palytoxin.

Referencias bibliográficas

  • Ciminiello P, Dell'Aversano C, Fattorusso E, Forino M, Tartaglione L, Grillo C, Melchiorre N (2008) Putative palytoxin and its new analogue, ovatoxin-a, in Ostreopsis ovata collected along the Ligurian coasts during the 2006 toxic outbreak. J Am Soc Mass Spectrom 19(1):111–120
  • Ciminiello P, Dell'Aversano C, Iacovo ED, Fattorusso E, Forino M, Grauso L, Tartaglione L, Guerrini F, Pistocchi R (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(18):2735–2744
  • Ciminiello P, Dellaversano C, Iacovo ED, Fattorusso E, Forino M, Tartaglione L, Battocchi C, Crinelli R, Carloni E, Magnani M, Penna A (2012) Unique toxin profile of a Mediterranean Ostreopsis cf. ovata strain: HR LC-MSn characterization of ovatoxin-f, a new palytoxin congener. Chem Res Toxicol 25(6):1243–1252
  • Munday R (2011) Palytoxin toxicology: animal studies. Toxicon 57(3):470–477
  • Moore RE, Bartolini G (1981) Structure of palytoxin. J Am Chem Soc 103(9):2491–2494
  • Uemura D, Ueda K, Hirata Y, Naoki H, Iwashita T (1981) Further studies on palytoxin. II. Structure of palytoxin. Tetrahedron Lett 22(29):2781–2784
  • Crinelli R, Carloni E, Giacomini E, Penna A, Dominici S, Battocchi C, Ciminiello P, Dell'Aversano C, Fattorusso E, Forino M (2012) Palytoxin and an Ostreopsis toxin extract increase the levels of mRNAs encoding inflammation-related proteins in human macrophages via p38 MAPK and NF-kB. PLoS One 7(6):e38139
  • Durando P, Ansaldi F, Oreste P, Moscatelli P, Marensi L, Grillo C, Gasparini R, Icardi G (2007) Ostreopsis ovata and human health: epidemiological and clinical features of respiratory syndrome outbreaks from a two-year syndromic surveillance, 2005–06, in north-west Italy. Euro Surveill 12 (23): http://www.eurosurveillance.org/ViewArticle.aspx?ArticleId=3212 . Accessed June 3210, 2014
  • Mangialajo L, Ganzin N, Accoroni S, Asnaghi V, Blanfuné A, Cabrini M, Cattaneo-Vietti R, Chavanon F, Chiantore M, Cohu S (2011) Trends in Ostreopsis proliferation along the Northern Mediterranean coasts. Toxicon 57(3):408–420
  • Tubaro A, Durando P, Del Favero G, Ansaldi F, Icardi G, Deeds J, Sosa S (2011) Case definitions for human poisonings postulated to palytoxins exposure. Toxicon 57(3):478–495
  • Casabianca S, Casabianca A, Rioboó P, Franco JM, Vila M, Penna A (2013) Quantification of the toxic dinoflagellate Ostreopsis spp. by qPCR assay in marine aerosol. Environ Sci Technol 47(8):3788–3795
  • Ciminiello P, Dell'Aversano C, Iacovo ED, Fattorusso E, Forino M, Tartaglione L, Benedettini G, Onorari M, Serena F, Battocchi C, Casabianca S, Penna A (2014) First finding of Ostreopsis cf. ovata toxins in marine aerosols. Environ Sci Technol 48(6):3532–3540. doi: 10.1021/es405617d
  • Ciminiello P, Dell’Aversano C, Fattorusso E, Forino M, Magno GS, Tartaglione L, Grillo C, Melchiorre N (2006) The Genoa 2005 outbreak. Determination of putative palytoxin in Mediterranean Ostreopsis ovata by a new liquid chromatography tandem mass spectrometry method. Anal Chem 78:6153–6159
  • Ciminiello P, Dell'Aversano C, Dello Iacovo E, Fattorusso E, Forino M, Grauso L, Tartaglione L, Guerrini F, Pezzolesi L, Pistocchi R, Vanucci S (2012) Isolation and structure elucidation of ovatoxin-a, the major toxin produced by Ostreopsis ovata. J Am Chem Soc 134(3):1869–1875
  • Brissard C, Herrenknecht C, Séchet V, Hervé F, Pisapia F, Harcouet J, Lémée R, Chomérat N, Hess P, Amzil Z (2014) Complex toxin profile of French Mediterranean Ostreopsis cf. ovata strains, seafood accumulation and ovatoxins prepurification. Mar Drugs 12(5):2851–2876
  • Suzuki T, Watanabe R, Uchida H, Matsushima R, Nagai H, Yasumoto T, Yoshimatsu T, Sato S, Adachi M (2012) LC-MS/MS analysis of novel ovatoxin isomers in several Ostreopsis strains collected in Japan. Harmful Algae 20:81–91
  • 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(17):1999–2008
  • Ciminiello P, Dell'Aversano C, Dello Iacovo E, Fattorusso E, Forino M, Grauso L, Tartaglione L (2012) Stereochemical studies on ovatoxin-a. Chem Eur J 18(52):16836–16843
  • Ciminiello P, Dell'Aversano C, Iacovo ED, Fattorusso E, Forino M, Tartaglione L (2011) LC-MS of palytoxin and its analogues: state of the art and future perspectives. Toxicon 57(3):376–38920
  • Ciminiello P, Dell'Aversano C, Iacovo ED, Fattorusso E, Forino M, Grauso L, Tartaglione L (2012) High resolution LC-MSn fragmentation pattern of palytoxin as template to gain new insights into ovatoxin-A structure. The key role of calcium in MS behavior of palytoxins. J Am Soc Mass Spectrom 23(5):952–963
  • Vila M, Garcés E, Masó M (2001) Potentially toxic epiphytic dinoflagellate assemblages on macroalgae in the NW Mediterranean. Aquat Microb Ecol 26(1):51–60
  • Barroso García P, de la Puerta PR, Parrón Carreño T, Marín Martínez P, Guillén Enríquez J (2008) Brote con síntomas respiratorios en la provincia de Almería por una posible exposición a microalgas tóxicas. Gac Sanit 22(6):578–584
  • Riobó P, Paz B, Franco J (2006) Analysis of palytoxin-like in Ostreopsis cultures by liquid chromatography with precolumn derivatization and fluorescence detection. Anal Chim Acta 566(2):217–223
  • Pezzolesi L, Guerrini F, Ciminiello P, Dell'Aversano C, Dello Iacovo E, Fattorusso E, Forino M, Tartaglione L, Pistocchi R (2012) Influence of temperature and salinity on Ostreopsis cf. ovata growth and evaluation of toxin content through HR LC-MS and biological assays. Water Res 46(1):82–92
  • Hoshaw RW, Rosowski JR (1973) Methods for microscopic algae. In: Stein JR (ed) Handbook of phycological methods, vol 1. CUP Archive, pp 53–67
  • Andree KB, Fernández-Tejedor M, Elandaloussi LM, Quijano-Scheggia S, Sampedro N, Garcés E, Camp J, Diogène J (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(5):1651–1659
  • Sato S, Nishimura T, Uehara K, Sakanari H, Tawong W, Hariganeya N, Smith K, Rhodes L, Yasumoto T, Taira Y (2011) Phylogeography of Ostreopsis along west Pacific coast, with special reference to a novel clade from Japan. PLoS One 6(12):e27983
  • Utermöhl VH (1931) Neue Wege in der quantitativen Erfassung des Planktons. Verh Int Ver Theor Angew Limnol 5:567–596
  • Accoroni S, Romagnoli T, Colombo F, Pennesi C, di Camillo CG, Marini M, Battocchi C, Ciminiello P, Dell'Aversano C, Dello Iacovo E, Fattorusso E, Tartaglione L, Penna A, Totti C (2011) Ostreopsis cf. ovata bloom in the northern Adriatic Sea during summer 2009: ecology, molecular characterization and toxin profile. Mar Pollut Bull 62(11)):2512–2519
  • Guerrini F, Pezzolesi L, Feller A, Riccardi M, Ciminiello P, Dell'Aversano C, Tartaglione L, Iacovo ED, Fattorusso E, Forino M (2010) Comparative growth and toxin profile of cultured Ostreopsis ovata from the Tyrrhenian and Adriatic Seas. Toxicon 55(2):211–220
  • Honsell G, De Bortoli M, Boscolo S, Dell'Aversano C, Battocchi C, Fontanive G, Penna A, Berti F, Sosa S, Yasumoto T (2011) Harmful dinoflagellate Ostreopsis cf. ovata Fukuyo: detection of ovatoxins in field samples and cell immunolocalization using antipalytoxin antibodies. Environ Sci Technol 45(16):7051–7059
  • Rossi R, Castellano V, Scalco E, Serpe L, Zingone A, Soprano V (2010) New palytoxin-like molecules in Mediterranean Ostreopsis cf. ovata (dinoflagellates) and in Palythoa tuberculosa detected by liquid chromatography–electrospray ionization time-of-flight mass spectrometry. Toxicon 56(8):1381–1387