Skip to main content
SpringerLink
Log in

Morphology, phylogeny, and toxicity of Atama complex (Dinophyceae) from the Chukchi Sea

  • Original Paper
  • Published:
Polar Biology Aims and scope Submit manuscript

Abstract

The “Atama complex”, which consists of Alexandrium tamarense, A. fundyense, and A. catenella, is one of the most important groups within the dinoflagellate genus Alexandrium. Information of the biogeography of the Atama complex is limited in the Arctic Ocean. In the present study, we established 55 strains of the Atama complex by incubating ellipsoidal cysts collected from the Chukchi Sea. The vegetative cells are characterized by a prominent ventral pore, thereby fitting the description of A. tamarense morphotype. Large subunit (LSU) and/or internal transcribed spacer (ITS) region sequences of these strains were examined. Both sequences showed intragenomic polymorphism. The 708 bp of the LSU sequences from the strains differed from each other at 0–44 sites (0.0–6.2 %), and the ITS region sequences differed from one another at 0–28 sites (0.0–5.4 %). Phylogenetic analysis revealed that the Chukchi Sea strains were nested within Atama complex (Group I). Assessment of paralytic shellfish poisoning toxin production by four Chukchi Sea strains using high-performance liquid chromatography showed that total toxin per cell ranged from 9 to 41 fmol cell−1. The toxin profile of the four strains from the Chukchi Sea is conserved, with the major toxins being N-sulfocarbamoyl toxin (C2), saxitoxin, and gonyautoxin-4. Our results support that dispersal of the Atama complex (Group I) from the Bering Sea to the Chukchi Sea might have occurred.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Adachi M, Sako Y, Ishida Y (1996) Analysis of Alexandrium (Dinophyceae) species using sequences of the 5.8S ribosomal DNA and internal transcribed spacer regions. J Phycol 32:424–432

    Article  CAS  Google Scholar 

  • Aguilera-Belmonte A, Inostroza I, Franco JM, Riobó P, Gómez PI (2011) The growth, toxicity and genetic characterization of seven strains of Alexandrium catenella (Whedon and Kofoid) Balech 1985 (Dinophyceae) isolated during the 2009 summer outbreak in southern Chile. Harmful Algae 12:105–112

    Article  Google Scholar 

  • Alpermann T, Tillmann U, Beszteri B, Cembella A, John U (2010) Phenotypic variation and genotypic diversity in a planktonic population of the toxigenic marine dinoflagellate Alexandrium tamarense (Dinophyceae). J Phycol 46:18–32

    Article  CAS  Google Scholar 

  • Alverson AJ, Kolnick L (2005) Intragenomic nucleotide polymorphism among small subunit (18S) rDNA paralogs in the diatom genus Skeletonema (Bacillariophyta). J Phycol 41:1248–1257

    Article  CAS  Google Scholar 

  • Anderson D, Kulis D, Doucette G, Gallagher J, Balech E (1994) Biogeography of toxic dinoflagellates in the genus Alexandrium from the northeastern United States and Canada. Mar Biol 120:467–478

    Article  Google Scholar 

  • Anderson DM, Stock CA, Keafer BA, Bronzino Nelson A, Thompson B, McGillicuddy DJ, Keller M, Matrai PA, Martin J (2005) Alexandrium fundyense cyst dynamics in the Gulf of Maine. Deep-Sea Res Pt II 52:2522–2542

    Article  Google Scholar 

  • Anderson DM, Alpermann TJ, Cembella AD, Collos Y, Masseret E, Montresor M (2012) The globally distributed genus Alexandrium: multifaceted roles in marine ecosystems and impacts on human health. Harmful Algae 14:10–35

    Article  PubMed  Google Scholar 

  • Baggesen C, Moestrup Ø, Daugbjerg N, Krock B, Cembella D, Madsen S (2012) Molecular phylogeny and toxin profiles of Alexandrium tamarense (Lebour) Balech (Dinophyceae) from the west coast of Greenland. Harmful Algae 19:108–116

    Google Scholar 

  • Bolch CJS, De Salas MF (2007) A review of the molecular evidence for ballast water introduction of the toxic dinoflagellates Gymnodinium catenatum and the Alexandrium. Harmful Algae 6:465–485

    Article  CAS  Google Scholar 

  • Brosnahan ML, Kulis DM, Solow AR, Erdner DL, Percy L, Lewis J, Anderson DM (2010) Outbreeding lethality between toxic Group I and non toxic Group III Alexandrium tamarense spp. isolates: predominance of heterotypic encystment and implications formatting interactions and biogeography. Deep-Sea Res Pt II 57:175–189

    CAS  Google Scholar 

  • Burrell S, Gunnarsson T, Gunnarsson K, Clarke D, Turner AD (2012) First detection of paralytic shellfish poisoning (PSP) toxins in Icelandic mussels (Mytilus edulis): links to causative phytoplankton species. Food Control. http://dx.doi.org/10.1016/j.foodcont.2012.10.002

  • Cembella AD (1998) Ecophysiology and metabolism of paralytic shellfish toxins in marine microalgae. In: Anderson DM, Cembella AD, Hallegraeff GM (eds) Physiological ecology of harmful algal blooms, NATO-Advanced Study Institute Series, vol 41. Springer, Heidelberg, pp 381–404

    Google Scholar 

  • Clark PU, Dyke AS, Shakun JD, Carlson AE, Clark J, Wohlfarth B, Mitrovica JX, Hostetler SW, McCabe AM (2009) The last glacial maximum. Science 325:710–714

    Article  PubMed  CAS  Google Scholar 

  • Coachman LK, Aagaard K (1966) On the water exchange through Bering Strait. Limnol Oceanogr 11:44–59

    Article  Google Scholar 

  • Coleman AW (2007) Pan-eukaryote ITS2 homologies revealed by RNA secondary structure. Nucleic Acids Res 35:3322–3329

    Article  PubMed  CAS  Google Scholar 

  • Collins C, Graham J, Brown L, Bresnan E, Lacaze JP, Turrell E (2009) Identification and toxicity of Alexandrium tamarense (Dinophyceae) in Scottish waters. J Phycol 45:692–703

    Article  Google Scholar 

  • Crespo BG, Keafer BA, Ralston DK, Lind H, Farber D, Anderson DM (2011) Dynamics of Alexandrium fundyense blooms and shellfish toxicity in the Nauset Marsh System of Cape Cod (Massachusetts, USA). Harmful Algae 12:26–38

    Article  Google Scholar 

  • Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792–1797

    Article  PubMed  CAS  Google Scholar 

  • Fritz L, Triemer R (1985) A rapid simple technique utilizing calcofluor white M2R for the visualization of dinoflagellate thecal plates. J Phycol 21:662–664

    Article  Google Scholar 

  • Ganley ARD, Kobayashi T (2007) Highly efficient concerted evolution in the ribosomal DNA repeats: total rDNA repeat variation revealed by whole-genome shotgun sequence data. Genome Res 17:184–191

    Article  PubMed  CAS  Google Scholar 

  • Genovesi B, Laabir M, Masseret E, Collos Y, Vaquer A, Grzebyk D (2009) Dormancy and germination features in resting cysts of Alexandrium tamarense species complex (Dinophyceae) can facilitate bloom formation in a shallow lagoon (Thau, southern France). J Plankton Res 31:1209–1224

    Article  Google Scholar 

  • Gribble KE, Anderson DM (2007) High intraindividual, intraspecific, and interspecific variability in large-subunit ribosomal DNA in the heterotrophic dinoflagellates Protoperidinium, Diplopsalis, and Preperidinium (Dinophyceae). Phycologia 46:315–324

    Article  Google Scholar 

  • Guillard RRL, Ryther JH (1962) Studies of marine planktonic diatoms. I. Cyclotella nana Hustedt and Detonula confervacea Cleve. Can J Microbiol 8:229–239

    Article  PubMed  CAS  Google Scholar 

  • Hoffert MI, Covey C (1992) Deriving global climate sensitivity from palaeoclimate reconstructions. Nature 360:573–576

    Article  Google Scholar 

  • John U, Fensome RA, Medlin LK (2003) The application of a molecular clock based on molecular sequences and the fossil record to explain biogeographic distributions within the Alexandrium tamarense “species complex” (Dinophyceae). Mol Biol Evol 20:1015–1027

    Article  PubMed  CAS  Google Scholar 

  • Kim YO, Park MH, Han MS (2002) Role of cyst germination in the bloom initiation of Alexandrium tamarense (Dinophyceae) in Masan Bay, Korea. Aquat Microb Ecol 29:279–286

    Article  Google Scholar 

  • Kim CJ, Yoshihiko S, Aritsune U, Kim CH (2004) Molecular phylogenetic relationships within the genus Alexandrium (Dinophyceae) based on the nuclear-encoded SSU and LSU rDNA D1–D2 sequences. J Kor Soc Oceanogr 39:172–185

    Google Scholar 

  • Lilly E, Kulis D, Gentien P, Anderson D (2002) Paralytic shellfish poisoning toxins in France linked to a human-introduced strain of Alexandrium catenella from the western Pacific: evidence from DNA and toxin analysis. J Plankton Res 24:443–452

    Article  CAS  Google Scholar 

  • Lilly EL, Halanych KM, Anderson DM (2007) Species boundaries and global biogeography of the Alexandrium tamarense complex (Dinophyceae). J Phycol 43:1329–1338

    Article  CAS  Google Scholar 

  • Macintyre J, Cullen J, Cembella A (1997) Vertical migration, nutrition and toxicity in the dinoflagellate Alexandrium tamarense. Mar Ecol Prog Ser 148:201–216

    Article  Google Scholar 

  • Marret F, Zonneveld KAF (2003) Atlas of modern organic-walled dinoflagellate cyst distribution. Rev Palaeobot Palynol 125:1–200

    Article  Google Scholar 

  • Medlin LK, Lange M, Wellbrock U, Donner G, Elbrächter M, Hummert C, Luckas B (1998) Sequence comparisons link toxic European isolates of Alexandrium tamarense from the Orkney Islands to toxic North American stocks. Eur J Protistol 34:329–335

    Article  Google Scholar 

  • Miranda LN, Zhuang Y, Zhang H, Lin S (2012) Phylogenetic analysis guided by intragenomic SSU rDNA polymorphism refines classification of “Alexandrium tamarense” species complex. Harmful Algae 16:35–48

    Article  CAS  Google Scholar 

  • Moestrup Ø, Hansen PJ (1988) On the occurrence of the potentially toxic dinoflagellates Alexandrium tamarense (=Gonyaulax excavata) and A. ostenfeldii in Danish and Faroese waters. Ophelia 28:195–213

    Article  Google Scholar 

  • Montresor M, Lovejoy C, Orsini L, Procaccini G, Roy S (2003) Bipolar distribution of the cyst-forming dinoflagellate Polarella glacialis. Polar Biol 26:186–194

    Google Scholar 

  • Murata A, Nagashima Y, Taguchi S (2012) N:P ratios controlling the growth of the marine dinoflagellate Alexandrium tamarense: content and composition of paralytic shellfish poison. Harmful Algae. doi:10.1016/j.hal.2012.07.001

    Google Scholar 

  • Niemi A, Michel C, Hille K, Poulin M (2011) Protist assemblages in winter sea ice: setting the stage for the spring ice algal bloom. Polar Biol 34:1803–1807

    Article  Google Scholar 

  • Oppen MJHV, Diekmann O, Wiencke C, Stam W, Olsen J (1994) Tracking dispersal routes phylogeography of the Arctic–Antarctic disjunct seaweed Acrosiphonia arcta (Chlorophyta). J Phycol 30:67–80

    Article  Google Scholar 

  • Orlova TY, Selina MS, Lilly EL, Kulis DM, Anderson DM (2007) Morphogenetic and toxin composition variability of Alexandrium tamarense (Dinophyceae) from the east coast of Russia. Phycologia 46:534–548

    Article  Google Scholar 

  • Orr RJS, Stüken A, Rundberget T, Eikrem W, Jakobsen KS (2011) Improved phylogenetic resolution of toxic and non-toxic Alexandrium strains using a concatenated rDNA approach. Harmful Algae 10:676–688

    Article  Google Scholar 

  • Penna A, Garcés E, Vila M, Giacobbe MG, Fraga S, Luglié A, Bravo I, Bertozzini E, Vernesi C (2005) Alexandrium catenella (Dinophyceae), a toxic ribotype expanding in the NW Mediterranean Sea. Mar Biol 148:13–23

    Article  Google Scholar 

  • Persich GR, Kulis DM, Lilly EL, Anderson DM, Garcia VMT (2006) Probable origin and toxin profile of Alexandrium tamarense (Lebour) Balech from southern Brazil. Harmful Algae 5:36–44

    Article  CAS  Google Scholar 

  • Posada D (2008) jModelTest: phylogenetic model averaging. Mol Biol Evol 25:1253–1256

    Article  PubMed  CAS  Google Scholar 

  • Poulin M, Daugbjerg N, Gradinger R, Ilyash L, Ratkova T, von Quillfeldt C (2011) The pan-Arctic biodiversity of marine pelagic and sea-ice unicellular eukaryotes: a first-attempt assessment. Mar Biodivers 41:13–28

    Article  Google Scholar 

  • Ratkova TN, Wassmann P (2005) Sea ice algae in the White and Barents seas: composition and origin. Polar Res 24:95–110

    Article  Google Scholar 

  • Rodriguez F, Oliver J, Marin A, Medina JR (1990) The general stochastic model of nucleotide substitution. J Theor Biol 142:485–501

    Article  PubMed  CAS  Google Scholar 

  • Ronquist F, Huelsenbeck J (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574

    Article  PubMed  CAS  Google Scholar 

  • Scholin CA, Anderson DM, Sogin ML (1993) Two distinct small-subunit ribosomal RNA genes in the North American toxic dinoflagellate Alexandrium fundyense (Dinophyceae). J Phycol 29:209–216

    Article  CAS  Google Scholar 

  • Scholin CA, Herzog M, Sogin M, Anderson DM (1994) Identification of group- and strain-specific genetic markers for globally distributed Alexandrium (Dinophyceae). II. Sequence analysis of a fragment of the LSU rRNA gene. J Phycol 30:999–1011

    Article  CAS  Google Scholar 

  • Scholin C, Hallegraeff G, Anderson D (1995) Molecular evolution of the Alexandrium tamarense ‘species complex’ (Dinophyceae): dispersal in the North American and West Pacific regions. Phycologia 34:472–485

    Article  Google Scholar 

  • Sebastián CR, 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 44:49–60

    Article  Google Scholar 

  • Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739

    Article  PubMed  CAS  Google Scholar 

  • Tang Y, Jiao Y, Zou E (2001) A Preliminary analysis of the hydrographic features and water masses in the Bering Sea and the Chukchi Sea. Chin J Polar Res 13:57–68 (in Chinese)

    CAS  Google Scholar 

  • Thornhill DJ, Lajeunesse TC, Santos SR (2007) Measuring rDNA diversity in eukaryotic microbial systems: how intragenomic variation, pseudogenes, and PCR artifacts confound biodiversity estimates. Mol Ecol 16:5326–5340

    Article  PubMed  CAS  Google Scholar 

  • Varela D, Paredes J, Alves-de-Souza C, Seguel M, Sfeir A, Frangópulos M (2012) Intraregional variation among Alexandrium catenella (Dinophyceae) strains from southern Chile: morphological, toxicological and genetic diversity. Harmful Algae 15:8–18

    Article  CAS  Google Scholar 

  • Wang D, Hsieh DPH (2001) Dynamics of C2 toxin and chlorophyll-a formation in the dinoflagellate Alexandrium tamarense during large scale cultivation. Toxicon 39:1533–1536

    Article  PubMed  Google Scholar 

  • Weise AM, Levasseur M, Saucier FJ, Senneville S, Bonneau E, Roy S, Sauvé G, Michaud S, Fauchot J (2002) The link between precipitation, river runoff, and blooms of the toxic dinoflagellate Alexandrium tamarense in the St. Lawrence. Can J Fish Aquat Sci 59:464–473

    Article  Google Scholar 

  • Woodgate RA, Aagaard K, Weingartiner TJ (2005) Monthly temperature, salinity, and transport variability of the Bering Strait through flow. Geophys Res Lett 32:L04601. doi:10.1029/2004GL021880

    Article  Google Scholar 

Download references

Acknowledgments

We thank Dieter Piepenburg and three anonymous reviewers for constructive suggestions to improve the manuscript. This work was supported by the China Program for International Polar Year 2007–2011, the Special Research Foundation for Public Welfare Marine Program (201105022-2), and the National Natural Science Foundation of China (40476053).

Author information

Authors and Affiliations

  1. Third Institute of Oceanography, SOA, Xiamen, 361005, China

    Haifeng Gu, Ni Zeng & Weiguo Wang

  2. State Key Laboratory of Marine Environmental Science, Environmental Science Research Center, Xiamen University, Xiamen, 361005, China

    Zhangxian Xie & Dazhi Wang

  3. College of Life Science and Technology, Jinan University, Guangzhou, 510632, China

    Weidong Yang

Authors
  1. Haifeng Gu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ni Zeng
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Zhangxian Xie
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Dazhi Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Weiguo Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Weidong Yang
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Haifeng Gu or Dazhi Wang.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Cite this article

Gu, H., Zeng, N., Xie, Z. et al. Morphology, phylogeny, and toxicity of Atama complex (Dinophyceae) from the Chukchi Sea. Polar Biol 36, 427–436 (2013). https://doi.org/10.1007/s00300-012-1273-5

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00300-012-1273-5

Keywords

Search

Navigation