Advertisement

Marine Biology

, Volume 148, Issue 1, pp 13–23 | Cite as

Alexandrium catenella (Dinophyceae), a toxic ribotype expanding in the NW Mediterranean Sea

  • A. Penna
  • E. Garcés
  • M. Vila
  • M. G. Giacobbe
  • S. Fraga
  • A. Lugliè
  • I. Bravo
  • E. Bertozzini
  • C. Vernesi
Research Article

Abstract

The presence of the paralytic shellfish poisoning (PSP) dinoflagellate Alexandrium catenella in the north western (NW) Mediterranean Sea has been known since 1983. From this date on, the species has spread along the Spanish and Italian coastlines. Information concerning A. catenella isolates in the NW Mediterranean Sea was gained through phylogenetic studies. Twenty established toxic cultures of A. catenella taken from various NW Mediterranean Sea locations were analysed by nucleotide sequencing of the 5.8S rDNA and internal transcribed spacer regions. These rDNA ribosomal markers resulted useful in delineating the phylogenetic position of this species in the genus Alexandrium as well as in determining relationships between A. catenella isolates from different geographic areas. The phylogenetic position of the Mediterranean A. catenella ribotype, when compared to the “Alexandrium tamarense/catenella/fundyense species complex”, fits this species complex well. All the Mediterranean A.catenella isolates were constituted by only one genetic ribotype. By comparing the isolate sequences with those of other geographic areas, it revealed that the Mediterranean A. catenella ribotype was closely related to the A. catenella from Japan, Western Pacific Ocean. It was also evident that in temperate Japanese waters, a genetic variability was detected within A. catenella isolates; in fact, all strains resulted divergent showing as many as 15 mutational steps. The possibility that A. catenella has been recently introduced into the Mediterranean basin from temperate Asian areas is discussed.

Keywords

Ballast Water Paralytic Shellfish Poisoning Japanese Isolate North Western Isolate Sequence 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgements

This study was supported by the EU-FP5 Strategy Project EVK3-CT- 00046-2001 and CCVIEO. Special thanks to Dr. Mercedes Masò, Prof. Mauro Magnani and Dr. Francesca Andreoni for technical assistance in sequence analyses and to José M. Franco and CRM (Centro Ricerche Marine, Cesenatico, Italy) for providing toxin information and also to Kostantinos Koukaras for supplying a culture strain.

References

  1. Abadie E, Amzil Z, Belin C, Comps MA, Elzière-Papayanni P, Lassus P, LeBec C, Marcaillou-Le Baut C, Nézan E, Poggi R (1999) Contamination de l’étang de Thau par Alexandrium tamarense. Épisode de novembre à décembre 1998. Report Observation et surveillance de la mer côtière. Ifremer, Pluzané, p 44Google Scholar
  2. Adachi M, Sako Y, Ishida Y (1994) Restriction fragment length polymorphism of ribosomal DNA internal transcribed spacer and 5.8S regions in Japanese Alexandrium species (Dinophyceae). J Phycol 30:857–865CrossRefGoogle Scholar
  3. Adachi M, Sako Y, Ishida Y (1996) Analyses of Alexandrium (Dinophyceae) species using sequences of the 5.8S ribosomal DNA and internal transcribed spacer regions. J Phycol 32:424–432CrossRefGoogle Scholar
  4. Balech E (1995) The Genus Alexandrium Halim (Dinoflagellata). Sherkin Island Marine Station, Sherkin Island Co., Cork, IrelandGoogle Scholar
  5. Benavides H, Prado L, Diaz S, Carreto Jj (1995) An exceptional bloom of Alexandrium catenella in the Beagle Channel, Argentina. In: Lassus P, Arzul G, Erard-Le Denn E, Gentien P, Marcaillou-Le Baut C (eds) Harmful marine algal blooms. Proliferation D’algues Marines Nuisibles. Lavoisier, Paris, pp 113–119Google Scholar
  6. Clement M, Posada D, Crandall KA (2000) TCS: a computer program to estimate gene genealogies. Mol Ecol 9:1657–1659CrossRefGoogle Scholar
  7. Cordova JL, Muller I (2002) Use of PCR and partial sequencing of the large-subunit rRNA gene to identify Alexandrium catenella (Dinophyceae) from the South of Chile. Harmful Algae 1:343–350CrossRefGoogle Scholar
  8. Fernández R, Mamán L, Jaén D, Márquez I (2004) Control y seguimiento del fitoplancton tóxico en las costas anadaluzas durante los años 2001 y 2002. In: Norte M, Fernández R (eds) VII Reunión Ibérica sobre Fitoplancton Tóxico y biotoxinas. Instituto Universitario de Biorgánica de la Universidad de la Laguna. La Laguna, pp 99–107Google Scholar
  9. Figueroa RI, Bravo I, Garcés E (2005) Effects of nutritional factors and different parental crosses on the encystment and excystment of Alexandrium catenella in culture. Phycologia (in press)Google Scholar
  10. Garcés E, Masó M, Vila M, Camp J (2000) HABs events in the Mediterranean Sea: are they increasing? A case study of the last decade in the NW Mediterranean and the genus Alexandrium. Harmful Algal News 20:1–11Google Scholar
  11. Gomis C, Alcober J, Bernabeu A (1996) Seguimiento de las poblaciones fitoplanctonicas en las bateas mrjilloneras del Puerto de Valencia 1991–1994. In: Matamoros E, Delgado M (eds) IV Reunion Iberica de fitoplancton toxico y biotoxinas St. Carles de la Rapita (Tarragona): Generalitat de Catalunya. Department d’Agricultura, Ramaderia i Pesca, pp 29–38Google Scholar
  12. Guillard RRL (1975) Culture of phytoplankton for feeding marine invertebrates. In: Smith WL, Chanley MH (eds) Culture of marine invertebrate animals. Plenum Press, New York, pp 26–60Google Scholar
  13. Guillard RRL, Hargraves PE (1993) Stichochrysis inmobilis is a diatom, not a chrysophyte. Phycologia 32:234–236CrossRefGoogle Scholar
  14. Guillou L, Nézan E, Cueff V, Erard-Le Denn E, Cambon-Bonavita MA, Gentien P, Barbier G (2002) Genetic diversity and molecular detection of three toxic dinoflagellate genera (Alexandrium, Dinopysis and Karenia) from the French Coasts. Protist 153:223–238CrossRefGoogle Scholar
  15. Hallegraeff GM, Bolch CJ, Blackburn SI, Oshima Y (1991) Species of toxigenic dinoflagellate genus Alexandrium in south-eastern Australian waters. Bot Mar 34:575–587CrossRefGoogle Scholar
  16. Hallegraeff GM (1998) Transport of toxic dinoflagellates via ships’ ballast water: bioeconomic risk assessment and efficacy of possible ballast water management strategies. Mar Ecol Progr Ser 168:297–309CrossRefGoogle Scholar
  17. Higman WA, Stone DM, Lewis JM (2001) Sequence comparisons of toxic and non-toxic Alexandrium tamarense (Dinophyceae) isolates from UK waters. Phycologia 40:256–262CrossRefGoogle Scholar
  18. Huelsenbeck JP, Ronquist F (2001) MrBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17:754–755CrossRefGoogle Scholar
  19. John U, Fensome R, Medlin LK (2003) The application of a molecular clock based on molecular sequences and the fossil record to explain biogeographic distribution within the Alexandrium tamarense “Species Complex” (Dinophyceae). Mol Biol Evol 20:1015–1027CrossRefGoogle Scholar
  20. Karplus K, Barrett C, Hughey R (1998) Hidden markov models for detecting remote protein homologies. Bioinformatics 14:846–856CrossRefGoogle Scholar
  21. Keller MD, Selvin RC, Claus W, Guillard RRL (1987) Media for the culture of oceanic ultraphytoplankton. J Phycol 23:633–638CrossRefGoogle Scholar
  22. Kooistra WHCF, de Boer MK, Vrieling EG, Connell LB, Gieskes WC (2001) Variation along the ITS markers across strains of Fibrocapsa japonica (Raphidophyceae) suggests hybridization events and recent range expansion. J Sea Res 46:213–222CrossRefGoogle Scholar
  23. Kumar S, Tamura K, Jacobsen IB, Nei M (2001) MEGA 2: Molecular Evolutionary Genetics Analysis Software. Arizona State University, Tempe, AZ, USAGoogle Scholar
  24. Laabir M, Gentien P (1999) Survival of toxic dinoflagellates after gut passage in the Pacific oyster Crassostrea gigas Thunburg. J Shell Res 18:217–222Google Scholar
  25. Lilly EL, Kulis DM, Gentien P, Anderson DM (2002) Paralytic shellfish poisoning toxins in France linked to a human-introduced strain of Alexandrium catenella from western Pacific: evidence from DNA and toxin analysis. J Plank Res 24:443–452CrossRefGoogle Scholar
  26. Lugliè A, Giacobbe MG, Sannio A, Fiocca F, Sechi N (2003b) First record of the dinoflagellate Alexandrium catenella (Whedon & Kofoid) Balech (Dinophyta), a potential producer of paralytic shellfish poisoning, in Italian waters (Sardinia, Tyrrhenian Sea). Bocconea 16:1045–1052Google Scholar
  27. Lugliè A, Giacobbe MG, Sannio A, Fiocca F, Sechi N (2003a) The geographical distribution of Alexandrium catenella is extending to Italy! First evidences from the Tyrrhenian Sea. In: Proceeding of Xth international conference on Harmful Algae (in press)Google Scholar
  28. MacKenzie L, de Salas M, Adamson J, Beuzenberg V (2004) The dinoflagellate genus Alexandrium (Halim) in New Zealand coastal waters: comparative morphology, toxicity and molecular genetics. Harmful Algae 3:71–92CrossRefGoogle Scholar
  29. Mandal RK (1984) The organisation and transcription of eukaryotic ribosomal RNA genes. Progr Nucl Acid Res Mol Biol 31:115–158CrossRefGoogle Scholar
  30. Manhart JR, McCourt RM (1992) Molecular data and species concepts in the algae. J Phycol 28:730–737CrossRefGoogle Scholar
  31. Margalef R, Estrada M (1987) Synoptic distribution of summer microplankton (Algae and Protozoa) across the principal front in the Western Mediterranean. Investigaciones Pesqueria 51:121–140Google Scholar
  32. Masò M, Garcés E, Pagès F, Camp J (2003) Drifting plastic debris as a potential vector for dispersing Harmful Algal Bloom (HAB) species. Sci Mar 67:107–111CrossRefGoogle Scholar
  33. Masselin P, Amzil Z, Abadie E, Nézan E, Le Bec C, Carreras A, Chiantella C, Truquet P (2001) Paralytic shellfish poisoning on the French Mediterranean coast in autumn 1998: Alexandriumtamarense complex” (Dinophyceae) as causative agent. In: Hallegraeff GM, Blackburn SI, Bolch CJ, Lewis RJ (eds) Harmful Algal blooms 2000. Proceedings of IXth international conference harmful algal blooms, UNESCO, Paris, pp 26–29Google Scholar
  34. Medlin LK, Lange M, Wellbrock U, Donner G, Elbrachter M, Hummert C, Luckas B (1998) Sequence comparison link toxic European isolates of Alexandrium tamarense from the Orkney Islands to toxic North American stocks. Eur J Protistol 34:329–335CrossRefGoogle Scholar
  35. Mikhail SK (2001) Toxic red tide species are on rise in Alexandria waters (Egypt). Harmful Algae News 22:5Google Scholar
  36. Orsini L, Procaccini G, Sarno D, Montresor M (2004) Multiple rDNA ITS-type within the diatom Pseudo-nitzschia delicatissima (Bacillariophyceae) and their relative abundance across a spring bloom in the Gulf of Naples. Mar Ecol Progr Ser 271:87–98CrossRefGoogle Scholar
  37. Penna A, Magnani M (1999) Identification of Alexandrium (Dinophyceae) species using PCR and rDNA-targeted probes. J Phycol 35:615–621CrossRefGoogle Scholar
  38. Posada D, Crandall KA (1998) Modeltest: testing the model of DNA substitution. Bioinformatics 14:817–818CrossRefGoogle Scholar
  39. Rodriguez-Lanetty M, Krupp DA, Weis VM (2004) Distinct ITS types of Symbiodinium in Clade C correlate with cnidarian/dinoflagellate specificity during onset of symbiosis. Mar Ecol Progr Ser 275:97–102CrossRefGoogle Scholar
  40. Ruiz Sebastián C, Etheridge SM, Cook PA, O’Ryan C, Pitcher GC (2005) Phylogenetic analysis of toxic Alexandrium (Dinophyceae) isolates from South Africa: implications for the global phylogeography of the Alexandrium tamarense species complex. Phycologia (in press)Google Scholar
  41. Sampedro N, Vila M, Arín L, Garcés E, Camp J (2003) Seguimiento del fitoplancton tóxico en la costa catalana: incidencias durante 2000–2002. In: VIII Reunión Ibérica de fitoplancton Tóxico y Biotoxinas. La Laguna, Tenerife, pp 29–38Google Scholar
  42. Saunders GW, Hill DRA, Sexton JP, Andersen RA (1997) Small-subunit ribosomal RNA sequences from selected dinoflagellates: testing classical evolutionary hypotheses with molecular systematic methods. Plant System Evol 11:237–259CrossRefGoogle Scholar
  43. Scholin CA, Anderson DM (1994) Identification of group and strain-specific genetic markers for globally distributed Alexandrium (Dinophyceae). I RFLP analysis of SSUrRNA genes. J Phycol 30:744–754CrossRefGoogle Scholar
  44. Scholin CA, Herzog M, Sogin M, Anderson DM (1994) Identification of group-and strain — specific genetic markers for globally distributed Alexandrium (Dinophyceae). 2. Sequence analysis of a fragment of the LSU rRNA gene. J Phycol 30:999–1011CrossRefGoogle Scholar
  45. Scholin CA, Hallegraeff GM, Anderson DM (1995) Molecular evolution of the Alexandrium tamarense “species complex” (Dinophyceae): dispersal in the North American and West Pacific regions. Phycologia 34:472–485CrossRefGoogle Scholar
  46. Smayda TJ (1997) What is a bloom? A commentary. Limnol Oceanogr 42:1132–1136CrossRefGoogle Scholar
  47. Sournia A (1995) Red-tide and toxic marine phytoplankton of the world ocean: an inquiry into biodiversity Harmful Toxic Algal Blooms. Lavosier, Paris, pp 239–243Google Scholar
  48. Swofford DL (2000) PAUP*: phylogenetic analysis using parsimony (* and other methods), version. 4.0b. Sinauer Associates, SunderlandGoogle Scholar
  49. Tamura K, Nei M (1993) Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol Biol Evol 10:512–526Google Scholar
  50. Templeton AR, Crandall KA, Sing CF (1992) A cladistic analysis of phenotypic associations with haplotypes inferred from restriction endonuclease mapping and DNA sequence data. III. Cladogram estimation. Genetics 132:619–633PubMedPubMedCentralGoogle Scholar
  51. Usup G, Pin LC, Ahmad A, Teen LP (2002) Phylogenetic relationship of Alexandrium tamiyavanichii (Dinophyceae) to other Alexandrium species based on ribosomal RNA gene sequences. Harmful Algae 1:59–68CrossRefGoogle Scholar
  52. Vernesi C, Pecchioli E, Caramelli D, Tiedemann R, Randi E, Bertorelle G (2002) The genetic structure of natural and reintroduced roe deer (Capreolus capreolus) populations in the Alps and central Italy, with reference to the mitochondrial DNA phylogeography of Europe. Mol Ecol 11:1285–1297CrossRefGoogle Scholar
  53. Yeung PKK, Wong FTW, Wong JTY (2002) Large subunit rDNA sequences from Alexandrium catenella strains isolated during algal blooms in Hong Kong. J Appl Phycol 14:147–150CrossRefGoogle Scholar
  54. Vila M, Camp J, Garces E, Masó M, Delgado M (2001a) High resolution spatio-temporal detection of HABs in confined waters of the NW Mediterranean. J Plank Res 23:497–514CrossRefGoogle Scholar
  55. Vila M, Garces E, Masó M, Camp J (2001b) Is the distribution of the toxic dinoflagellate Alexandrium catenella expanding along the NW Mediterranean coast? Mar Ecol Progr Ser 222:73–83CrossRefGoogle Scholar
  56. Vila M, Delgado M, Camp J (2001c) First detection of widespread toxic events caused by Alexandrium catenella in the Mediterranean Sea. In: Hallegraeff GM, Blackburn SI, Bolch CJ, Lewis RJ (eds) Harmful Agal Blooms (2000) Proceedings of IXth International Harmful Algal Blooms. UNESCO, Paris, pp 8–11Google Scholar
  57. Vila M, Masó M (2005) Phytoplankton functional groups and harmful algal species in antropogenically impacted waters of the NW Mediterranean Sea. Sci Mar 69:31–45CrossRefGoogle Scholar
  58. Wendel JF, Schnabel A, Seelan T (1995) Bidirectional interlocus concerted evolution following allopolypoid speciation in cotton (Gossypium). Proc Natl Acad Sci USA 92:280–284CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2005

Authors and Affiliations

  • A. Penna
    • 1
  • E. Garcés
    • 2
  • M. Vila
    • 2
  • M. G. Giacobbe
    • 3
  • S. Fraga
    • 4
  • A. Lugliè
    • 5
  • I. Bravo
    • 4
  • E. Bertozzini
    • 1
  • C. Vernesi
    • 6
  1. 1.Centro Biologia AmbientaleUniversity of UrbinoPesaroItaly
  2. 2.Institut de Ciències del MarBarcelonaSpain
  3. 3.Istituto per l’Ambiente Marino CostieroCNRMessinaItaly
  4. 4.Instituto Español de OceanografíaVigoSpain
  5. 5.Dip. Botanica ed Ecologia VegetaleUniversity of SassariSassariItaly
  6. 6.Centro di Ecologia AlpinaViote del Monte BondoneTrentoItaly

Personalised recommendations