Abstract
Marine benthic dinoflagellates in the genus Coolia were reported in both tropical and temperate regions. We conducted a morphological and phylogenetic characterization of Coolia species from Hainan Island, South China Sea. The morphologies of three Coolia species were similar to those of the original descriptions of Coolia canariensis, C. tropicalis, and C. malayensis. In phylogenetic analyses based on the LSU rDNA and ITS regions (ITS1-5.8S-ITS2), the Hainan strains of C. canariensis, C. tropicalis, and C. malayensis clustered within the clades of these species with other isolates from different areas. No differences (p-distance) in LSU rDNA sequences were found between the Hainan C. malayensis strains and the strains from New Zealand, Florida of USA, Malaysia, Japan, Dominican Republic and Guangxi and Hong Kong of China. For C. canariensis and C. tropicalis, no differences (p-distance) in the LSU rDNA sequences were found between the Hainan strains (D1C2 and DS5F4, respectively) and the Australian strains (NQAIF252 and NQAIF90, respectively). Our study reveals the morphological and genetic diversity of Coolia species from Hainan Island, South China Sea, which provides a detailed understanding of Coolia species of this area.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data Availability Statement
The data that support the findings of this study are available on request from the corresponding author.
References
David H, Laza-Martínez A, Miguel I, Orive E. 2014. Broad distribution of Coolia monotis and restricted distribution of Coolia cf. canariensis (Dinophyceae) on the Atlantic coast of the Iberian Peninsula. Phycologia, 53(4): 342–352, https://doi.org/10.2216/13-214.1.
David H, Laza-Martínez A, Rodríguez F, Fraga S, Orive E. 2020. Coolia guanchica sp. nov. (Dinophyceae) a new epibenthic dinoflagellate from the Canary Islands (NE Atlantic Ocean). European Journal of Phycology, 55(1): 76–88, https://doi.org/10.1080/09670262.2019.1651400.
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. Scientia Marina, 70(1): 67–76, https://doi.org/10.3989/scimar.2006.70n167.
Faust M A. 1992. Observations on the morphology and sexual reproduction of Coolia monotis (Dinophyceae). Journal of Phycology, 28(1): 94–104, https://doi.org/10.1111/j.0022-3646.1992.00094.x.
Faust MA. 1995. Observation of sand-dwelling toxic dinoflagellates (Dinophyceae) from widely differing sites, including two new species. Journal of Phycology, 31(6): 996–1003, https://doi.org/10.1111/j.0022-3646.1995.00996.x.
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. Journal of Phycology, 44(4): 1 060–1 070, https://doi.org/10.1111/j.1529-8817.2008.00555.x.
Fukuyo Y. 1981. Taxonomical study on benthic dinoflagellates collected in coral reefs. Nippon Suisan Gakkaishi, 47(8): 967–978, https://doi.org/10.2331/suisan.47.967.
GEOHAB. 2012. global Ecology and Oceanography of Harmful Algal Blooms, GEOHAB Core Research Project: HABs in Benthic Systems. In: Berdalet E, Tester P, Zingone A eds. IOC of UNESCO and SCOR, Paris and Newark, 64pp.
Guillard R R L, Hargraves P E. 1993. Stichochrysis immobilis is a diatom, not a chrysophyte. Phycologia, 32(3): 234–236, https://doi.org/10.2216/i0031-8884-32-3-234.1.
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 Science Journal, 49(3): 211–221, https://doi.org/10.1007/s12601-014-0021-x.
Holmes M J, Lewis R J, Jones A, Hoy A W W. 1995. Cooliatoxin, the first toxin from Coolia monotis (Dinophyceae). Natural Toxins, 3(5): 355–362, https://doi.org/10.1002/nt.2620030506.
Hoppenrath M, Murray S A, Chomérat N, Horiguchi T. 2014. Marine Benthic Dinoflagellates—Unveiling Their Worldwide Biodiversity. Kleine Senckenberg-Reihe, Band 54, Schweizerbart, Stuttgart, Germany, 276pp.
Jeong H J, Yih W, Kang N S, Lee S Y, Yoon E Y, Yoo Y D, Kim H S, Kim J H. 2012. First report of the epiphytic benthic dinoflagellates Coolia canariensis and Coolia malayensis in the waters off Jeju Island, Korea: morphology and rDNA sequences. The Journal of Eukaryotic Microbiology, 59(2): 114–133, https://doi.org/10.1111/j.1550-7408.2012.00610.x.
Karafas S J, Tomas C R. 2015. Further observations on the genetics and morphometrics of Coolia santacroce (Dinophyceae). Algae, 30(4): 275–280, https://doi.org/10.4490/algae.2015.30.4.275.
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, https://doi.org/10.1016/j.hal.2015.05.002.
Kofoid G A. 1909. On Peridinium steinii Jöngensen, with a note on the nomenclature of the skeleton of the Peridinidae. Archiv Protistenkunde, 16: 25–47.
Kumar S, Stecher G, Li M, Knyaz C, Tamura K. 2018. MEGA X: Molecular Evolutionary Genetics Analysis across computing platforms. Molecular Biology and Evolution, 35(6): 1 547–1 549, https://doi.org/10.1093/molbev/msy096.
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. European Journal of Phycology, 46(1): 45–65, https://doi.org/10.1080/09670262.2010.550387.
Leaw C P, Lim P T, Cheng 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). Journal of Phycology, 46(1): 162–171, https://doi.org/10.1111/j.1529-8817.2009.00778.x.
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 F, Usup G, Lim P T. 2016. New scenario for speciation in the benthic dinoflagellate genus Coolia (Dinophyceae). Harmful Algae, 55: 137–149, https://doi.org/10.1016/j.hal.2016.02.010.
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. Marine Pollution Bulletin, 124(2): 878–889, https://doi.org/10.1016/j.marpolbul.2017.01.017.
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, https://doi.org/10.1016/j.hal.2018.04.001.
Litaker R W, Vandersea M W, Kibler S R, Reece K S, Stokes N A, Lutzoni F M, Yonish B A, West M A, Black M N D, Tester P A. 2007. Recognizing dinoflagellate species using ITS rDNA sequences. Journal of Phycology, 43(2): 344–355, https://doi.org/10.1111/j.1529-8817.2007.00320.x.
Meunier A. 1919. Microplankton de la mer Flamande. III. Les Péridiniens. Mémoires du Musée Royal d’Histoire Naturelle de Belgique. Bruxelles: Hayez, imprimeur de l’Académie royale de Belgique, 8: 1–116.
Mohammad-Noor N, Moestrup Ø, 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. Journal of Phycology, 49(3): 536–545, https://doi.org/10.1111/jpy.12062.
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(10): e79278, https://doi.org/10.1371/journal.pone.0079278.
Nascimento S M, Da Silva RAF, 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. European Journal of Phycology, 54(3): 484–496, https://doi.org/10.1080/09670262.2019.1599449.
Nunn G B, Theisen B F, Christensen B, Arctander P. 1996. Simplicity-correlated size growth of the nuclear 28S ribosomal RNA D3 expansion segment in the crustacean order Isopoda. Journal of Molecular Evolution, 42(2): 211–223, https://doi.org/10.1007/BF02198847.
Nylander JAA. 2004. MrModeltest v2. Program distributed by the author. Evolutionary Biology Center, Uppsala University.
Penna A, Vila M, Fraga S, Giacobbe M G, Andreoni F, Riobó 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. Journal of Phycology, 41(1): 212–225, https://doi.org/10.1111/j.1529-8817.2005.04011.X.
Rhodes L, Smith K, Papiol G G, Adamson J, Harwood T, Munday R. 2014. Epiphytic dinoflagellates in sub-tropical New Zealand, in particular the genus Coolia Meunier. Harmful Algae, 34: 36–41, https://doi.org/10.1016/j.hal.2014.02.004.
Ronquist F, Huelsenbeck J P. 2003. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics, 19(12): 1 572–1 574, https://doi.org/10.1093/bioinformatics/btg180.
Scholin C A, Herzog M, Sogin M, Anderson D A. 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. Journal of Phycology, 30(6): 999–1011, https://doi.org/10.1111/j.0022-3646.1994.00999.x.
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. Phycological Research, 63(2): 125–133, https://doi.org/10.1111/pre.12074.
Ten-Hage L, Turquet J, Quod J P, Couté A. 2000. Coolia areolata sp. nov. (Dinophyceae), a new sand-dwelling dinoflagellate from the southwestern Indian Ocean. Phycologia, 39(5): 377–383.
Thompson J D, Higgins D G, Gibson T J. 1994. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Research, 22(22): 4 673–4 680, https://doi.org/10.1093/nar/22.22.4673.
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, https://doi.org/10.1016/j.hal.2015.02.009.
Zhang H, Li Y, Cen J Y, Wang H L, Cui L, Dong Y L, Lu S H. 2015. Morphotypes of Prorocentrum lima (Dinophyceae) from Hainan Island, South China Sea: morphological and molecular characterization. Phycologia, 54(5): 503–516, https://doi.org/10.2216/15-8.1.
Acknowledgment
We thank Dr. WANG Hualong for his help with sampling.
Author information
Authors and Affiliations
Corresponding author
Additional information
Supported by the National Natural Science Foundation of China (Nos. 41606176, 41576162, 41606175) and the IOC Yeosu Benthic Dinoflagellate Project
Supplementary materials
Rights and permissions
About this article
Cite this article
Zhang, H., Lü, S., Cen, J. et al. Morphology and molecular phylogeny of three species of Coolia (Dinophyceae) from Hainan Island, South China Sea. J. Ocean. Limnol. 39, 1020–1032 (2021). https://doi.org/10.1007/s00343-020-9326-z
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00343-020-9326-z