Browse > Article
http://dx.doi.org/10.4490/algae.2021.36.6.2

Characterization of Coolia spp. (Gonyaucales, Dinophyceae) from Southern Tunisia: first record of Coolia malayensis in the Mediterranean Sea  

Abdennadher, Moufida (National Institute of Marine Sciences and Technologies)
Zouari, Amel Bellaaj (National Institute of Marine Sciences and Technologies)
Medhioub, Walid (National Institute of Marine Sciences and Technologies)
Penna, Antonella (Department of Biomolecular Sciences, University of Urbino)
Hamza, Asma (National Institute of Marine Sciences and Technologies)
Publication Information
ALGAE / v.36, no.3, 2021 , pp. 175-193 More about this Journal
Abstract
This study provides the first report of the presence of Coolia malayensis in the Mediterranean Sea, co-occurring with C. monotis. Isolated strains from the Gulf of Gabès, Tunisia (South-eastern Mediterranean) were identified by morphological characterization and phylogenetic analysis. Examination by light and scanning electron microscopy revealed no significant morphological differences between the Tunisian isolates and other geographically distant strains of C. monotis and C. malayensis. Phylogenetic trees based on ITS1-5.8S-ITS2 and D1-D3/28S rDNA sequences showed that C. monotis strains clustered with others from the Mediterranean and Atlantic whereas the C. malayensis isolate branched with isolates from the Pacific and the Atlantic, therefore revealing no geographical trend among C. monotis and C. malayensis populations. Ultrastructural analyses by transmission electron microscopy revealed the presence of numerous vesicles containing spirally coiled fibers in both C. malayensis and C. monotis cells, which we speculate to be involved in mucus production.
Keywords
harmful benthic dinoflagellate; ITS; LSU rDNA; morphology; South-east Mediterranean Sea;
Citations & Related Records
연도 인용수 순위
  • Reference
1 Abdennadher, M., Bellaaj Zouari, A., Feki Sahnoun, W., Alverca, E., Penna, A. & Hamza, A. 2017. Ostreopsis cf. ovata in the Gulf of Gabes (south-eastern Mediterranean Sea): morphological, molecular and ecological characterization. Harmful Algae 63:56-67.   DOI
2 Abdennadher, M., Bellaaj Zouari, A., Feki Sahnoun, W., Dammak Walha, L., Mahfoudi, M. & Hamza, A. 2020. A long-term study on Coolia monotis distribution from the South-east Mediterranean Sea. Cont. Shelf. Res. 211:104267.   DOI
3 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. 30:857-865.   DOI
4 Adachi, R. & Fukuyo, Y. 1979. The thecal structure of a marine toxic dinoflagellate Gambierdiscus toxicus gen. et sp. nov. collected in a ciguatera-endemic area. Bull. Jpn. Soc. Sci. Fish. 45:67-71.   DOI
5 Larsson, M. E., Smith, K. F. & Doblin, M. A. 2019. First description of the environmental niche of the epibenthic dinoflagellate species Coolia palmyrensis, C. malayensis, and C. tropicalis (Dinophyceae) from Eastern Australia. J. Phycol. 55:565-577.   DOI
6 Leaw, C. P., Lim, P. T., Ahmad, A. & Usup, G. 2001. Genetic diversity of Ostreopsis ovata (Dinophyceae) from Malaysia. Mar. Biotechnol. 3:246-255.   DOI
7 Karafas, S., York, R. & Tomas, C. 2015. Morphological and genetic analysis of the Coolia monotis species complex with the introduction of two new species, Coolia santacroce sp. nov. and Coolia palmyrensis sp. nov. (Dinophyceae). Harmful Algae 46:18-33.   DOI
8 Kumar, S., Stecher, G., Li, M., Knyaz, C. & Tamura, K. 2018. MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol. Biol. Evol. 35:1547-1549.   DOI
9 Leaw, C. -P., Lim, P. -T., Chen, K. -W., Ng, B. -K. & Usup, G. 2010. Morphology and molecular characterization of a new species of thecate benthic dinoflagellate, Coolia malayensis sp. nov. (Dinophyceae). J. Phycol. 46:162-171.   DOI
10 Leaw, C. P., Tan, T. H., Lim, H. C., Teng, S. T., Yong, H. L., Smith, K. F., Rhodes, L., Wolf, M., Holland, W. C., Vandersea, M. W., Litaker, R. W., Tester, P. A., Gu, H., Usup, G. & Lim, P. T. 2016. New scenario for speciation in the benthic dinoflagellate genus Coolia (Dinophyceae). Harmful Algae 55:137-149.   DOI
11 David, H., Laza-Martinez, A., Rodriguez, F., Fraga, S. & Orive, E. 2019. Coolia guanchica sp. nov. (Dinophyceae) a new epibenthic dinoflagellate from the Canary Islands (NE Atlantic Ocean). Eur. J. Phycol. 55:76-88.   DOI
12 Faust, M. A. 2009. Ciguatera-causing dinoflagellates in a coral-reef mangrove ecosystem, Belize. Atoll Res. Bull. 569:1-32.   DOI
13 Gomez, F. 2006. Endemic and Indo-Pacific plankton in the Mediterranean Sea: a study based on dinoflagellate records. J. Biogeogr. 33:261-270.   DOI
14 David, H., Laza-Martinez, A., Miguel, I. & Orive, E. 2014. Broad distribution of Coolia monotis and restricted distribution of Coolia cf. canariensis (Dinophyceae) in the Atlantic coast of the Iberian Peninsula. Phycologia 53:342-352.   DOI
15 Balech, E. 1956. Etude des Dinoflagelles du sable de Roscoff. Rev. Algol. 2:29-52.
16 Lewis, N. I., Wolny, J. L., Achenbach, J. C., Ellis, L., Pitula, J. S., Rafuse, C., Rosales, D. S. & McCarron, P. 2018. Identification, growth and toxicity assessment of Coolia Meunier (Dinophyceae) from Nova Scotia, Canada. Harmful Algae 75:45-56.   DOI
17 Loukil-Baklouti, A., Feki-Sahnoun, W., Hamza, A., Abdennadher, M., Mahfoudhi, M., Bouain, A. & Jarboui, O. 2018. Controlling factors of harmful microalgae distribution in water column, biofilm and sediment in shellfish production area (South of Sfax, Gulf of Gabes) from southern Tunisia. Cont. Shelf Res. 152:61-70.   DOI
18 Dolapsakis, N. P., Kilpatrick, M. W., Economou-Amilli, A. & Tafas, T. 2006. Morphology and rDNA phylogeny of a Mediterranean Coolia monotis (Dinophyceae) strain from Greece. Sci. Mar. 70:67-76.
19 Andersen, R. A. 2005. Algal culturing techniques. Elsevier Academic Press, Burlington, MA, 565 pp.
20 Armi, Z., Turki, S., Trabelsi, E. & Maiz, N. B. 2010. First recorded proliferation of Coolia monotis (Meunier, 1919) in the North Lake of Tunis (Tunisia) correlation with environmental factors. Environ. Monit. Assess. 164:423-433.   DOI
21 Ben-Gharbia, H., Yahia, O. K. -D., Amzil, Z., Chomerat, N., Abadie, E., Masseret, E., Sibat, M., Triki, H. Z., Nouri, H. & Laabir, M. 2016. Toxicity and growth assessments of three thermophilic benthic dinoflagellates (Ostreopsis cf. ovata, Prorocentrum lima and Coolia monotis) developing in the southern Mediterranean basin. Toxins 8:297.   DOI
22 Ben Ismail, S., Sammari, C., Gasparini, G. P., Beranger, K., Brahim, M. & Aleya, L. 2012. Water masses exchanged through the Channel of Sicily: evidence for the presence of new water masses on the Tunisian side of the channel. Deep Sea Res. I Oceanogr. Res. Pap. I 63:65-81.   DOI
23 Besada, E. G., Loeblich, L. A. & Loeblich, A. R. 3rd. 1982. Observations on tropical, benthic dinoflagellates from ciguatera-endemic areas: Coolia, Gambierdiscus, and Ostreopsis. Bull. Mar. Sci. 32:723-735.
24 Bianchi, C. N. & Morri, C. 2000. Marine biodiversity of the Mediterranean Sea: situation, problems and prospects for future research. Mar. Pollut. Bull. 40:367-376.   DOI
25 Galil, B. S. 2009. Taking stock: inventory of alien species in the Mediterranean Sea. Biol. Invasions 11:359-372.   DOI
26 Faust, M. A. 1995. Observation of sand-dwelling toxic dinoflagellates (Dinophyceae) from widely differing sites, including two new species. J. Phycol. 31:996-1003.   DOI
27 Felsenstein, J. 1981. Evolutionary trees from DNA sequences: a maximum likelihood approach. J. Mol. Evol. 17:368-376.   DOI
28 Fredj, G., Bellan-Santin, D. & Meinardi, M. 1992. Etat des connaissances sur la faune marine mediterraneenne. Bull. l'Inst. Oceanogr. Monaco 9:133-145.
29 Claparede, E. & Lachmann, J. 1859. Etudes sur les infusoires et les rhizopodes. Mem. l'Inst. Natl. Genev. 6:261-482.
30 Calic, M., Ljubimir, S., Bosak, S. & Car, A. 2018. First records of two planktonic Indo-Pacific diatoms: Chaetoceros bacteriastroides and C. pseudosymmetricus in the Adriatic Sea. Oceanologia 60:101-105.   DOI
31 Dammak-Zouari, H., Hamza, A. & Bouain, A. 2009. Gymnodiniales in the Gulf of Gabes (Tunisia). Cah. Biol. Mar. 50:153-170.
32 Ho, T. V. & Nguyen, L. N. 2014. Morphology and distribution of the three epiphytic dinoflagellate species Coolia monotis, C. tropicalis, and C. canariensis (Ostreopsidaceae, Gonyaulacales, Dinophyceae) from Vietnamese coastal waters. Ocean Sci. J. 49:211-221.   DOI
33 Gomez, F., Echevarria, F., Garcia, C. M., Prieto, L., Ruiz, J., Reul, A., Jimenez-Gomez, F. & Varela, M. 2000. Microplankton distribution in the Strait of Gibraltar: coupling between organisms and hydrodynamic structures. J. Plankton Res. 22:603-617.   DOI
34 Giussani, V., Sbrana, F., Asnaghi, V., Vassalli, M., Faimali, M., Casabianca, S., Penna, A., Ciminiello, P., Dell'Aversano, C., Tartaglione, L., Mazzeo, A. & Chiantore, M. 2015. Active role of the mucilage in the toxicity mechanism of the harmful benthic dinoflagellate Ostreopsis cf. ovata. Harmful Algae 44:46-53.   DOI
35 Gomez, F. 2003a. Checklist of Mediterranean free-living dinoflagellates. Bot. Mar. 46:215-242.   DOI
36 Gomez, F. 2003b. The toxic dinoflagellate Gymnodinium catenatum: an invader in the Mediterranean Sea. Acta Bot. Croat. 62:65-72.
37 Fraga, S., Penna, A., Bianconi, I., Paz, B. & Zapata, M. 2008. Coolia canariensis sp. nov. (Dinophyceae), a new nontoxic epiphytic benthic dinoflagellate from the Canary Islands. J. Phycol. 44:1060-1070.   DOI
38 Al-Yamani, F. Y. & Saburova, M. A. 2010. Illustrated guide on the flagellates of Kuwait's intertidal soft sediments. Kuwait Institute for Scientific Research, Safat, 197 pp.
39 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.   DOI
40 Ben Ismail, S., Schroeder, K., Sammari, C., Gasparini, G. P., Borghinic, M. & Aleya, L. 2014. Interannual variability of water mass properties in the Tunisia-Sicily Channel. J. Mar. Syst. 135:14-28.   DOI
41 Holmes, M. J., Lewis, R. J., Jones, A. & Hoy, A. W. 1995. Cooliatoxin, the first toxin from Coolia monotis (Dinophyceae). Nat. Toxins 3:355-362.   DOI
42 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. 10:512-526.
43 Scholin, C. A., Herzog, M., Sogin, M. & Anderson, D. M. 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.   DOI
44 Shah, M. M. R., Samarakoon, K. W., Ko, J. -Y., Chaminda Lakmal, H. H., Lee, J. -H., An, S. -J., Jeon, Y. -J. & Lee, J. -B. 2014. Potentiality of benthic dinoflagellate cultures and screening of their bioactivities in Jeju Island, Korea. Afr. J. Biotechnol. 13:792-805.   DOI
45 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.
46 Tawong, W., Nishimura, T., Sakanari, H., Sato, S., Yamaguchi, H. & Adachi, M. 2015. Characterization of Gambierdiscus and Coolia (Dinophyceae) isolates from Thailand based on morphology and phylogeny. Phycol. Res. 63:125-133.   DOI
47 Penna, A., Vila, M., Fraga, S., Giacobbe, M. G., Andreoni, F., Riobo, P. & Vernesi, C. 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.   DOI
48 Laza-Martinez, 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.   DOI
49 Leung, P. T. Y., Yan, M., Yiu, S. K. F., Lam, V. T. T., Ip, J. C. H., Au, M. W. Y., Chen, C. -Y., Wai, T. -C. & Lam, P. K. S. 2017. Molecular phylogeny and toxicity of harmful benthic dinoflagellates Coolia (Ostreopsidaceae, Dinophyceae) in a sub-tropical marine ecosystem: the first record from Hong Kong. Mar. Pollut. Bull. 124:878-889.   DOI
50 Pagliara, P. & Caroppo, C. 2012. Toxicity assessment of Amphidinium carterae, Coolia cfr. monotis and Ostreopsis cfr. ovata (Dinophyta) isolated from the northern Ionian Sea (Mediterranean Sea). Toxicon 60:1203-1214.   DOI
51 Reynolds, C. S. 2007. Variability in the provision and function of mucilage in phytoplankton: facultative responses to the environment. Hydrobiologia 578:37-45.   DOI
52 Rhodes, L., Smith, K., Harwood, T. & Bedford, C. 2014a. Novel and toxin-producing epiphytic dinoflagellates isolated from sub-tropical Raoul Island, Kermadec Islands group. N. Z. J. Mar. Freshw. Res. 48:594-599.   DOI
53 Rhodes, L. L. & Thomas, A. E. 1997. Coolia monotis (Dinophyceae): a toxic epiphytic microalgal species found in New Zealand (note). N. Z. J. Mar. Freshw. Res. 31:139-141.   DOI
54 Mendes, M. C. Q., Nunes, J. M. C., Fraga, S., Rodriguez, F., Franco, J. M., Riobo, P., Branco, S. & Menezes, M. 2019. Morphology, molecular phylogeny and toxinology of Coolia and Prorocentrum strains isolated from the tropical South Western Atlantic Ocean. Bot. Mar. 62:125-140.   DOI
55 Ten-Hage, L., Turquet, J., Quod, J. P. & Coute, A. 2000. Coolia areolata sp. nov. (Dinophyceae), a new sand-dwelling dinoflagellate from the southwestern Indian Ocean. Phycologia 39:377-383.   DOI
56 Nguyen, N. L. & Larsen, J. 2004. Gonyaulacales. In Larsen, J. & Nguyen, N. L. (Eds.) Guide to the Identification of Potentially Toxic Microalgae in Vietnamese Waters. Opera Bot. 140, Copenhagen, pp. 73-116.
57 Gomez, F., Qiu, D., Otero-Morales, E., Lopes, R. M. & Lin, S. 2016. Circumtropical distribution of the epiphytic dinoflagellate Coolia malayensis (Dinophyceae): morphology and molecular phylogeny from Puerto Rico and Brazil. Phycol. Res. 64:194-199.   DOI
58 Guillard, R. R. L. & Hargraves, P. E. 1993. Stichochrysis inmobilis is a diatom, not a chrysophyte. Phycologia 32:234-236.   DOI
59 Halim, Y. 1960. Etude quantitative et qualitative du cycle ecologique des Dinoflagelles dans les eaux de Villefranche-sur-Mer. Ann. Inst. Oceanogr. 38:123-232.
60 Madeira, F., Park, Y. M., Lee, J., Buso, N., Gur, T., Madhusoodanan, N., Basutkar, P., Tivey, A. R. N., Potter, S. C, Finn, R. D. & Lopez, R. 2019. The EMBL-EBI search and sequence analysis tools APIs in 2019. Nucleic Acids Res. 47:W636-W641.   DOI
61 Meunier, A. 1919. Microplankton de la Mer Flamande. III. Les Peridiniens. Mem. Mus. R. Hist. Nat. Belg. 8:116-144.
62 Mikulski, C. M., Morton, S. L. & Doucette, G. J. 2005. Development and application of LSU rRNA probes for Karenia brevis in the Gulf of Mexico, USA. Harmful Algae 4:49-60.   DOI
63 Zhang, H., Lu, S., Cen, J., Li, Y., Li, Q. & Wu, Z. 2020. Morphology and molecular phylogeny of three species of Coolia (Dinophyceae) from Hainan Island, South China Sea. J. Oceanol. Limnol. Advanced publication. https://doi.org/10.1007/s00343-020-9326-z.   DOI
64 Tibirica, C. E. J. A., Sibat, M., Fernandes, L. F., Bilien, G., Chomerat, N., Hess, P. & Mafra, L. L. Jr. 2020. Diversity and toxicity of the genus Coolia Meunier in Brazil, and detection of 44-methyl gambierone in Coolia tropicalis. Toxins 12:327.   DOI
65 Vila, M., Garces, E. & Maso, M. 2001. Potentially epiphytic dinoflagellate assemblages on macroalgae in the NW Mediterranean. Aquat. Microbiol. Ecol. 26:51-60.   DOI
66 Wakeman, K. C., Yamaguchi, A., Roy, M. C. & Jenke-Kodama, H. 2015. Morphology, phylogeny and novel chemical compounds from Coolia malayensis (Dinophyceae) from Okinawa, Japan. Harmful Algae 44:8-19.   DOI
67 Nascimento, S. M., da Silva, R. A. F., Oliveira, F., Fraga, S. & Salgueiro, F. 2019. Morphology and molecular phylogeny of Coolia tropicalis, Coolia malayensis and a new lineage of the Coolia canariensis species complex (Dinophyceae) isolated from Brazil. Eur. J. Phycol. 54:484-496.   DOI
68 Mohammad Noor, N., Adam, A., Saad, S., Khodzori, F. A. & Shaleh, S. R. M. 2019. Substrate preference and effects of medium with soil extract on growth of genus Coolia (Dinophyceae). J. Sustain. Sci. Manag. 14:71-81.
69 Momigliano, P., Sparrow, L., Blair, D. & Heimann, K. 2013. The diversity of Coolia spp. (Dinophyceae Ostreopsidaceae) in the Central Great Barrier Reef Region. PLoS ONE 8:e79278.   DOI
70 Moncer, M., Hamza, A., Feki-Sahnoun, W., Mabrouk, L. & Bel Hassen, M. 2017. Variability patterns of epibenthic microalgae in eastern Tunisian coasts. Sci. Mar. 81:487-498.   DOI
71 Ismael, A. A. 2014. First record of Coolia monotis Meunier along Alexandria coast: Egypt. Egypt. J. Aquat. Res. 40: 19-25.   DOI
72 Office de la Marine Marchande et des Ports. 2019. Rapport annuel. Office de la Marine Marchande et des Ports, La Goulette, 46 pp.
73 Hallegraeff, G. M. 1993. A review of harmful algal blooms and their apparent global increase. Phycologia 32:79-99.   DOI
74 Hattour, A. & Ben Mustapha, K. 2013. Le couvert vegetal marin du golfe de Gabes: Cartographie et reseau de surveillance de l'herbier de Posidonie. Institut National des Sciences et Technologies de la Mer, Salammbo, 164 pp.
75 Haywood, A. J., Steidinger, K. A., Truby, E. W., Bergquist, P. R., Bergquist, P. L., Adamson, J. & MacKenzie, L. 2004. Comparative morphology and molecular phylogenetic analysis of three new species of the genus Karenia (Dinophyceae) from New Zealand. J. Phycol. 40:165-179.   DOI
76 Honsell, G., Bonifacio, A., De Bortoli, M., Penna, A., Battocchi, C., Ciminiello, P., Dell'Aversano, C., Fattorusso, E., Sosa, S., Yasumoto, T. & Tubaro, A. 2013. New insights on cytological and metabolic features of Ostreopsis cf. ovata Fukuyo (Dinophyceae): a multidisciplinary approach. PLoS ONE 8:e57291.   DOI
77 Rhodes, L., Smith, K., Papiol, G. G., Adamson, J., Harwood, T. & Munday, R. 2014b. Epiphytic dinoflagellates in subtropical New Zealand, in particular the genus Coolia Meuneir. Harmful Algae 34:36-41.   DOI
78 Mohammad-Noor, N., Moestrup, O., Lundholm, N., Fraga, S., Adam, A., Holmes, M. J. & Saleh, E. 2013. Autecology and phylogeny of Coolia tropicalis and Coolia malayensis (Dinophyceae), with emphasis on taxonomy of C. tropicalis based on light microscopy, scanning electron microscopy and LSU rDNA. J. Phycol. 49:536-545.   DOI