Morphology and molecular phylogeny of three species of Coolia (Dinophyceae) from Hainan Island, South China Sea

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, access via your institution.

References

  1. 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.

    Article  Google Scholar 

  2. 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.

    Article  Google Scholar 

  3. 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.

    Article  Google Scholar 

  4. 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.

    Article  Google Scholar 

  5. 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.

    Article  Google Scholar 

  6. 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.

    Article  Google Scholar 

  7. 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.

    Article  Google Scholar 

  8. 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.

  9. 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.

    Article  Google Scholar 

  10. 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.

    Article  Google Scholar 

  11. 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.

    Article  Google Scholar 

  12. 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.

    Google Scholar 

  13. 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.

    Article  Google Scholar 

  14. 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.

    Article  Google Scholar 

  15. 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.

    Article  Google Scholar 

  16. 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.

    Google Scholar 

  17. 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.

    Article  Google Scholar 

  18. 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.

    Article  Google Scholar 

  19. 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.

    Article  Google Scholar 

  20. 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.

    Article  Google Scholar 

  21. 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.

    Article  Google Scholar 

  22. 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.

    Article  Google Scholar 

  23. 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.

    Article  Google Scholar 

  24. 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.

    Google Scholar 

  25. 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.

    Article  Google Scholar 

  26. 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.

    Article  Google Scholar 

  27. 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.

    Article  Google Scholar 

  28. 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.

    Article  Google Scholar 

  29. Nylander JAA. 2004. MrModeltest v2. Program distributed by the author. Evolutionary Biology Center, Uppsala University.

  30. 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.

    Article  Google Scholar 

  31. 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.

    Article  Google Scholar 

  32. 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.

    Article  Google Scholar 

  33. 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.

    Article  Google Scholar 

  34. 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.

    Article  Google Scholar 

  35. 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.

    Article  Google Scholar 

  36. 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.

    Article  Google Scholar 

  37. 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.

    Article  Google Scholar 

  38. 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.

    Article  Google Scholar 

Download references

Acknowledgment

We thank Dr. WANG Hualong for his help with sampling.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Songhui Lü.

Additional information

Supported by the National Natural Science Foundation of China (Nos. 41606176, 41576162, 41606175) and the IOC Yeosu Benthic Dinoflagellate Project

Data Availability Statement

The data that support the fi ndings of this study are available on request from the corresponding author.

Supplementary materials

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

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. (2020). https://doi.org/10.1007/s00343-020-9326-z

Download citation

Keywords

  • Coolia
  • Hainan Island
  • morphology
  • phylogeny
  • rDNA