First molecular records of potentially harmful planktonic dinoflagellatesfrom the southern Black Sea
First molecular records of potentially harmful planktonic dinoflagellatesfrom the southern Black Sea
The aim of this study was to identify dinoflagellate species from the Black Sea (Samsun coast) using conventional and molecular phylogenetic methods. Water samples were collected using a plankton net with 22 μm pores. Dinoflagellate cells were documented under a light microscope and were then isolated for the single-cell PCR procedure. Phylogenetic inference showed that the isolates collected from the study area were affiliated with various harmful taxa: Dinophysis acuta Ehrenbergand Phalacroma rotundatum (Claparéde & Lachmann) Kofoid & Michener from dinophysioids, and Prorocentrum compressum (Bailey) Abé ex Dodge, P. cordatum (Ostenfeld) Dodge,and P. micans Ehrenbergfrom prorocentroids. In the phylogenetic tree we also observed that 2 of our gymnodiniod isolates were in a deep branch, indicating a cryptic genus of the family Kareniaceae. One of our isolates was related to the genus Peridiniella Kofoid & Michener of an uncertain family in Gonyaulacales. Network analyses of the DNA sequences were performed for phylogeographic investigation of the isolates. Five isolates are related to potentially harmful algal species. We have reported the first molecular data concerning these potentially harmful species from the Black Sea.
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- Baytut O, Gonulol A, Koray T (2010). Temporal variations of phytoplankton in relation to eutrophication in Samsun Bay, southern Black Sea. Turk J Fish Aquat Sc 10: 3-10.
- Bergholtz T, Daugbjerg N, Moestrup Ø, Fernández-Tejedor M (2006). On the identity of Karlodinium veneficum and the description of Karlodinium armiger sp. nov. (Dinophyceae), based on light and electron microscopy, nuclear-encoded LSU rDNA, and pigment composition. J Phycol 42: 170-193.
- Bodeanu N (1995). Algal bloom in Mamaia Bay (Romanian Black Sea coast), harmful marine algal blooms. In: Proceedings of the 6th International Conference on Toxic Marine Plankton, Technique and Documentation Lavosier, Nantes, pp. 127-137.
- Cembella AD (2003). Chemical ecology of eukaryotic microalgae in marine ecosystems. Phycologia 42: 420-447.
- Daugbjerg N, Hansen G, Larsen J, Moestrup Ø (2000). Phylogeny of some of the major genera of dinoflagellates based on ultrastructure and partial LSU rDNA sequence data, including the erection of three new genera of unarmoured dinoflagellates. Phycologia 39: 302-317.
- De Salas MF, Rhodes LL, MacKenzie LA, Adamson JE, Ponikla K (2005). Gymnodinioid genera Karenia and Takayama(Dinophyceae) in New Zealand coastal waters. New Zeal J Mar Fresh 39: 135-139.
- De Salas MF, Laza-Martinez A, Hallegraeff GM (2008). Novel unarmored dinoflagellates from the toxigenic family Kareniaceae (Gymnodiniales): five new species of Karlodiniumand one new Takayama from the Australian sector of the Southern Ocean. J Phycol 44: 241-257.
- Edvardsen B, Shalchian-Tabrizi K, Jakobsen KS, Medlin LK, Dahl E, Brubak S, Paasche E (2003). Genetic variability and molecular phylogeny of Dinophysis species (Dinophyceae) from Norwegian waters inferred from single cell analyses of rDNA. J Phycol 39: 395-408.
- European Commission 2002. Eutrophication and health. Luxembourg: Office for Official Publications of the European Communities.
- Fensome RA, Taylor FJR, Norris G, Sarjeant WAS, Williams GL (1993). A classification of living and fossil dinoflagellates. Micropaleontology 7: 1-349.
- GEOHAB, 2006. HABs in eutrophic systems. IOC-SCOR, 76s, Paris.
- Grzebyk D, Denardou A, Berland B, Pouchus YF (1997). Evidence of a new toxin in the red-tide dinoflagellate Prorocentrum minimum. J Plankton Res 19: 1111-1124.
- Gu H, Luo Z, Krock B, Witt M, Tillmann U (2013). Morphology, phylogeny and azaspiracid profile of Azadinium poporum(Dinophyceae) from the China Sea. Harmful Algae 21-22: 64-75.
- Guillou L, Nezan 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, Dinophysis, and Karenia) from French coasts. Protist 153: 223-238.
- Guindon S, Gascuel O (2003). A simple, fast and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52: 696-704.
- Hackett JD, Anderson DM, Erdner DL, Bhattacharya D (2004). Dinoflagellates: a remarkable evolutionary experiment. Am J Bot 91: 1523-1534.
- Hall TA (1999). BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl Acid S 41: 95-98.
- Hallegraeff GM (2004). Harmful algal blooms: a global overview. In: Hallegraeff GM, Anderson DM, Cembella AD, editors. Manual on Harmful Microalgae. France: UNESCO, pp. 25-50.
- Hart MC, Gren DH, Bresnan E, Bolch CJ (2007). Large subunit ribosomal RNA gene variation and sequence heterogeneity of Dinophysis (Dinophyceae) species from Scottish coastal waters. Harmful Algae 6: 271-287.
- Hastrup Jensen M, Daugbjerg N (2009). Molecular phylogeny of selected species of the order Dinophysiales (Dinophyceae)testing the hypothesis of a dinophysioid radiation. J Phycol 45: 1136-1152.
- Heil CA, Glibert PM, Fan C (2005). Prorocentrum minimum (Pavillard) Schiller: a review of a harmful algal bloom species of growing worldwide importance. Harmful Algae 4: 449-470.
- Henrichs DW, Scott PS, Steidinger KA, Errera RM, Abraham A, Campbell L (2013). Morphology and phylogeny of Prorocentrum texanum sp. nov. (Dinophyceae): a new toxic Dinoflagellate from the Gulf of Mexico coastal waters exhibiting two distinct morphologies. J Phycol 49: 143-155.
- Howard MD, Smith GJ, Kudela RM (2009). Phylogenetic relationships of yessotoxin-producing dinoflagellates, based on the large subunit and internal transcribed spacer ribosomal DNA domains. Appl Environ Microb 75: 54-63.
- Huson DH, Bryant D (2006). Application of phylogenetic networks in evolutionary studies. Mol Biol Evol 23: 254-267.
- Jensen MH, Daugbjerg N (2009). Molecular phylogeny of selected species of the order Dinophysiales (Dinophyceae)testing the hypothesis of a Dinophysioid radiation. J Phycol 45: 1136-1152.
- Librado P, Rozas J (2009). DnaSPv5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25: 1451-1452.
- Luo Z, Gu H, Krock B, Tillmann U (2013). Azadinium dalianense, a new dinoflagellate species from the Yellow Sea, China. Phycologia 52: 625-636.
- Moestrup Ø, Daugbjerg N (2007). On the dinoflagellate phylogeny and classification. In: Brodie J, Lewis J, editors. Unravelling the Algae: the Past, Present, and Future of Algal Systematics. Boca Raton, LA, USA: CRC Press, pp. 215-230.
- Mohammad-Noor N, Moestrup Ø, and Daugbjerg N (2007). Light, electron microscopy and DNA sequences of the dinoflagellate Prorocentrum concavum (syn. P. arabianum) with special emphasis on the periflagellar area. Phycologia 46: 549-564.
- Morton SL, Vershinin A, Smith LL, Leighfield LA, Pankov S, Quilliam MA (2009). Seasonality of Dinophysis spp. and Prorocentrum lima in Black Sea phytoplankton and associated shellfish toxicity. Harmful Algae 8: 629-636.
- Nezan E, Tillmann U, Bilien G, Boulben S, Cheze K, Zentz F, Salas R, Chomerat N (2012). Taxonomic revision of the dinoflagellate Amphidoma caudata: transfer to the genus Azadinium(Dinophyceae) and proposal of two varieties, based on morphological and molecular phylogenetic analyses. J Phycol 48: 925-939.
- Nezan E, Siano R, Boulben S, Six C, Bilien G, Cheze K, Duval A, Le Panse S, Quere J, Chomerat N (2014). Genetic diversity of the harmful family Kareniaceae (Gymnodiniales, Dinophyceae) in France, with the description of Karlodinium gentienii sp. nov.: a new potentially toxic dinoflagellate. Harmful Algae 40: 75-91.
- Nunn GB, Theisen BF, Christensen B, Arctander P (1996). Simplicity-correlated size growth of the nuclear 28S ribosomal RNA D3 expansion segment in the crustacean order Isopoda. J Mol Evol 42: 211-223.
- Pearce I, Hallegraeff GM (2004). Genetic affinities, ecophysiology and toxicity of Prorocentrum playfairii and P. foveolata(Dinophyceae) from Tasmanian freshwaters. Phycologia 43: 271-281.
- Posada D (2008). jModel test: phylogenetic model averaging. Mol Biol Evol 25: 1253-1256.
- Reguera B, Velo-Suarez L, Raine R, Park MG (2012). Harmful Dinophysis species: a review. Harmful Algae 14: 87-106.
- Rene A, de Salas M, Campa J, Balaguéa V, Garcés E (2013). A new clade, based on partial LSU rDNA sequences of unarmoured Dinoflagellates. Protist 164: 673-685.
- Rehnstam-Holm A-S, Godhe A, Anderson DM (2002). Molecular studies of Dinophysis (Dinophyceae) species from Sweden and North America. Phycologia 41: 348-357.
- Ronquist F, Huelsenbeck JP (2003). MRBAYES 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19: 1572-1574.
- Salas R, Tillmann U, John U, Kilcoyne J, Burson A, Cantwell C, Hess P, Jauffrais T, Silke J (2011). The role of Azadinium spinosum(Dinophyceae) in the production of azaspiracid shellfish poisoning in mussels. Harmful Algae 10: 774-783.
- Saldarriaga JF, Taylor FJ, Keeling PJ, Cavalier-Smith T (2001). Dinoflagellate nuclear SSU rRNA phylogeny suggests multiple plastid losses and replacements. J Mol Evol 53: 204-213.
- 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. In: BhattacharyaD, editor. Origins of Algae and their Plastids. New York, NY, USA: Springer-Verlag, pp. 237-259.
- 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 rDNA. J Phycol 30: 999-1011.
- Shankle AM (2001). Population variability in the red tide forming dinoflagellate, Prorocentrum micans. Thesis Scripps Institution of Oceanography, UCSD, La Jolla, CA, USA.
- Swofford DL (1998). PAUP*: phylogenetic analysis using parsimony (*and other methods). Version 4 beta 10. Sunderland, MA, USA: Sinauer Associates.
- Tang YZ, Kong L, Morse RE, Gobler CJ, Holmes MJ (2012). First report of a bloom-forming Dinoflagellate Takayama acrotrocha(Dinophyceae) from tropical coastal waters of Singapore. Journal Phycol 48: 455-466.
- Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997). The ClustalX-Windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25: 4876-4882.
- Tillmann U, Elbraechter M, John U, Krock B, Cembella A (2010). Azadinium obesum (Dinophyceae), a new nontoxic species in the genus that can produce azaspiracid toxins. Phycologia 49: 169-182.
- Tillmann U, Gottschling M, Nezan E, Krock B, Bilien G (2014). Morphological and molecular characterization of three new Azadinium species (Amphidomataceae, Dinophyceae) from the Irminger Sea. Protist 165: 417-444.
- Van den Hoek C, Mann DG, Jahns HM (1995). Algae: and Introduction to Phycology. Cambridge, UK: Cambridge University Press, 623 pp.
- Velikova V, Larsen J (1999). The Prorocentrum cordatum/Prorocentrum minimum taxonomic problem. Grana 38: 108-112.
- Yasumoto T, Murata M, Oshima Y, Sano M, Matsumoto G, Clardy J (1985). Diarrhetic shellfish toxins. Tetrahedron 41: 1019-1025.