Morphology and Molecular Characterisation of Karenia mikimotoi (Dinophyceae) from Sabah Malaysian Borneo, with a Focus on the Second Internal Transcribed Spacer (ITS2) of Ribosomal RNA gene

Characterisation of Karenia mikimotoi from Sabah

Authors

  • SHERYL UNCHA ANDREW CHIBA Faculty of Resource Science and Technology, Universiti Malaysia Sarawak, Kota Samarahan, 94300 Sarawak, Malaysia
  • SING TUNG TENG Faculty of Resource Science and Technology, Universiti Malaysia Sarawak, 94300 Kota Samarahan, Sarawak, Malaysia
  • SAMSUR MOHAMAD Faculty of Resource Science and Technology, Universiti Malaysia Sarawak, 94300 Kota Samarahan, Sarawak, Malaysia
  • NURSYAHIDA ABDULLAH Faculty of Resource Science and Technology, Universiti Malaysia Sarawak, 94300 Kota Samarahan, Sarawak, Malaysia
  • ING KUO LAW Faculty of Resource Science and Technology, Universiti Malaysia Sarawak, 94300 Kota Samarahan, Sarawak, Malaysia
  • PO TEEN LIM Bachok Marine Research Station, Institute of Ocean and Earth Sciences, University of Malaya, 16310 Bachok, Kelantan, Malaysia
  • CHUI PIN LEAW Bachok Marine Research Station, Institute of Ocean and Earth Sciences, University of Malaya, 16310 Bachok, Kelantan, Malaysia

DOI:

https://doi.org/10.33736/bjrst.7417.2024

Abstract

The first recorded bloom of Karenia mikimotoi (initially Gymnodinium mikimotoi) occurred off the coast of Japan in 1934, causing mass mortality of shellfish and fish. This event highlighted the devastating impact of K. mikimotoi blooms and marked a turning point in harmful algal bloom (HAB) research, driving studies on its identification, biology, toxicology, and effects on marine life and ecosystems. The past reported bloom events in Southeast Asia have raised public concerns, leading to further investigation into the occurrence and geographical distribution of K. mikimotoi in the region. As of yet, there is no recorded evidence of K. mikimotoi blooms in Malaysian waters. This prompt the investigation of the occurrence and distribution of K. mikimotoi in Malaysia, and this study represent the first record of K. mikimotoi in Malaysian waters. In this study, clonal cultures of K. mikimotoi isolated from Sepanggar Bay, Sabah were examined using light microscopy (LM) and scanning electron microscopy (SEM) to observe its morphological features. Cells of K. mikimotoi from Malaysian Borneo exhibited a typical dorso-ventrally flattened body with bi-lobed and linear apical grooves on the cell apex. Molecular characterisation of the strains based on the internal transcribed spacer (ITS) region and large-subunit (LSU) ribosomal DNA revealed close phylogenetic relationships with other strains of K. mikimotoi from other regions, forming a monophyletic clade that positioned as sister to K. brevis, supporting the species identity of K. mikimotoi. The secondary structure of the ITS2 RNA transcript revealed a universal structure with four major helices. Structural comparison between K. mikimotoi and its relatives revealed four to six hemi-compensatory base changes. The results demonstrated the efficacy of ITS2 secondary structure information in delimiting species in Karenia. The detailed morphology and molecular characteristics of K. mikimotoi were revealed, for the first time, from the coastal waters of Malaysian Borneo.

References

Ali, S.E., Mittal, A. & Mathews, D.H. (2023). RNA secondary structure analysis using RNAstructure. Current Protocols, 3, e846. DOI: 10.1002/cpz1.846

Amato, A., Kooistra, W.H., Ghiron, J.H., Mann, D.G., Pröschold, T., & Montresor, M. (2007). Reproductive isolation among sympatric cryptic species in marine diatoms. Protist, 158(2), 193–207. DOI: 10.1016/j.protis.2006.10.001

Azanza, R.V. & Benico, G.A. (2017). “Fish kills” in the Philippines associated with harmful algal blooms (HABs). Proceedings of the Tenth EASTHAB Symposium.

Babu, M.J., Geetha, P. & Soman, K.P. (2016). MODIS-aqua data based detection and classification of algal blooms along the coast of India using RLS classifier. Procedia Computer Science, 93, 424-430. DOI: 10.1016/j.procs.2016.07.238

Baohong, C., Kang, W., Huige, G. & Hui, L. (2021). Karenia mikimotoi blooms in coastal waters of China from 1998 to 2017. Estuarine, Coastal and Shelf Science, 249, 107034. DOI: 10.1016/j.ecss.2020.107034

Benico, G., Takahashi, K., Lum, W.M. & Iwataki, M. (2019). Morphological variation, ultrastructure, pigment composition and phylogeny of the star-shaped dinoflagellate Asterodinium gracile (Kareniaceae, Dinophyceae). Phycologia, 5(4), 405-418. DOI: 10.1080/00318884.2019.1601948

Bergholtz, T., Daugbjerg, N. & Fernández, M. (2006). On the identity of Karlodinium veneficum and description of Karlodinium armiger sp. nov. (Dinophyceae), based on light and electron microscopy, nuclear-encoded LSU rDNA, and pigment composition. Journal of Phycology, 42, 170-193. DOI: 10.1111/j.1529-8817.2006.00187.x

Botes, L., Sym, S. & Pitcher, G. (2003). Karenia cristata sp. nov. and Karenia bicuneiformis sp. nov. (Gymnodiniales, Dinophyceae): two new Karenia species from the South African Coast. Phycologia, 42, 563-571. DOI: 10.2216/i0031-8884-42-6-563.1

Caruana, A. M. N. & Amzil, Z. (2018). Chapter 13 - Microalgae and Toxins. In: Microalgae in Health and Disease Prevention (Levine, I. A. and Fleurence, J., 1st ed.), pp. 263-305. London: Academic Press.

Cen, J., Wang, J., Huang, L., Ding, G., Qi, Y., Cao, R., Cui, L. & Lü, S. (2020). Who is the “murderer” of the bloom in coastal waters of Fujian, China, in 2019? Journal of Oceanology and Limnology, 38, 722-732. DOI: 10.1007/s00343-020-9290-8

Cen, J., Lu, S., Moestrup, Ø., Jiang, T., Ho, K. C., Li, S., Li, M., Huan, Q. & Wang, J. (2024). Five Karenia species along the Chinese coast: with the description of a new species, Karenia hui sp. nov. (Kareniaceae, Dinophyta). Harmful Algae, 137, 102645. DOI: 10.1016/j.hal.2024.102645

Coleman, A.W. (2003). ITS2 is a double-edged tool for eukaryote evolutionary comparisons. Trends in Genetics, 19, 370-375. DOI: 10.1016/S0168-9525(03)00118-5

Coleman, A.W. (2009). Is there a molecular key to the level of “biological species” in eukaryotes? A DNA guide. Molecular Phylogenetics and Evolution, 50, 197-203. DOI: 10.1016/j.ympev.2008.10.008

D’Silva, M.S., Anil, A.C., Naik, R.K. & D’Costa, P.M. (2012). Algal blooms: a perspective from the coasts of India. Natural Hazards, 63, 1225-1253. DOI: 10.1007/s11069-012-0200-3

Darriba, D., Taboada, G.L., Doallo, R. & Posada, D. (2012). jModelTest 2: more models, new heuristics and parallel computing. Nature Methods, 9, 772. DOI: 10.1038/nmeth.2109

Darty, K., Denise, A., & Ponty, Y. (2009). VARNA: Interactive drawing and editing of the RNA secondary structure. Bioinformatics, 25(15), 1974–1975. DOI: 10.1093/bioinformatics/btp250

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. DOI: 10.2216/i0031-8884-39-4-302.1

Davis, C.C. (1948). Gymnodinium brevis sp. nov., a cause of discolored water and animal mortality in the Gulf of Mexico. Botanical Gazette, 109, 358-360. DOI: 10.1086/335561

de Salas, M.F., Bolch, C.J.S., Botes, L., Nash, G., Wright, S.W. & Hallegraeff, G.M. (2003). Takayama gen. nov. (Gymnodiniales, Dinophyceae), a new genus of unarmored dinoflagellates with sigmoid apical grooves, including the description of two new species. Journal of Phycology, 39, 1233-1246. DOI: 10.1111/j.0022-3646.2003.03-086.x

de Salas, M.F., Bolch, C.J.S. & Hallegraeff, G. M. (2004). Karenia umbella sp. nov. (Gymnodiniales, Dinophyceae), a new potentially ichthyotoxic dinoflagellate species from Tasmania, Australia. Phycologia, 43, 166-175. DOI: 10.2216/i0031-8884-43-2-166.1

Ericson, K. (2016). Making space for red tide: discoloured water and the early twentieth century bayscape of Japanese pearl cultivation. Journal of the History of Biology, 50, 393-423. DOI: 10.1007/s10739-016-9443-x

Escobar-Morales, S. & Hernández-Becerril, D. (2015). Free-living marine planktonic unarmoured dinoflagellates from the Gulf of Mexico and the Mexican Pacific. Botanica Marina, 58, 9-22. DOI: 10.1515/bot-2014-0084

Eunson, R. (1955). The Pearl King: The Fabulous Story of Mikimoto. New York: Greenberg.

Flewelling, L.J., Naar, J.P., Abbott, J.P., Baden, D.G., Barros, N.B., Bossart, G.D., Bottein, M.-Y.D., Hammond, D.G., Haubold, E.M., Heil, C.A., Henry, M.S., Jacocks, H.M., Leighfield, T.A., Pierce, R.H., Pitchford, T.D., Rommel, S.A., Scott, P.S., Steidinger, K.A., Truby, E.W., Van Dolah, F.M. & Landsberg, J.H. (2005). Red tides and marine mammal mortalities. Nature, 435, 755-756. DOI: 10.1038/nature435755a

Friedheim, S. (2016). Comparison of species identification methods: DNA barcoding versus morphological taxonomy. Journal of Microbiology & Experimentation, 3(1), 00082. DOI: 10.15406/jmen.2016.03.00082

Fukuyo, Y., Imai, I., Kodama, M. & Tamai, K. (2002). Red tides and other harmful algal blooms in Japan. In: Taylor, F. J. R. and Trainer, V. L. (eds.) Harmful algal blooms in the PICES region of the North Pacific. Sidney, B.C., Canada: Institute of Ocean Sciences.

Gentien, P. (1998). Bloom dynamics and ecophysiology of the Gymnodinium mikimotoi species complex. Physiological ecology of harmful algal blooms, 155-173.

Guiry, M.D. & Guiry, G.M. (2023). AlgaeBase. World-wide electronic publication. Available: https://www.algaebase.org.

Gunter, G., Williams, R.H., Davis, C.C. & Smith, F.G.W. (1948). Catastrophic mass mortality of marine animals and coincident phytoplankton bloom on the West Coast of Florida, November 1946 to August 1947. Ecological Monographs, 18, 309-324. DOI: 10.2307/1948622

Hansen, G., Daugbjerg., N. & Henriksen, P. (2000). Comparative study of Gymnodinium mikimotoi and Gymnodinium aureolum, comb. nov. (=Gyrodinium aureolum) based on morphology, pigment composition, and molecular data. Journal of Phycology, 36(2), 394-410. DOI: 10.1046/j.1529-8817.2000.99172.x

Hartman, S.E., Hartman, M.C., Hydes, D.J., Smythe-Wright, D., Gohin, F., & Lazure, P. (2014). The role of hydrographic parameters, measured from a ship of opportunity, in bloom formation of Karenia mikimotoi in the English Channel. Journal of Marine Systems, 139: 455-463. DOI: 10.1016/j.jmarsys.2014.07.001

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. Journal of Phycology, 40(1), 165-179. DOI: 10.1111/j.0022-3646.2004.02-149.x

Heil, C.A. & Steidinger, K.A. (2009). Monitoring, management, and mitigation of Karenia blooms in the eastern Gulf of Mexico. Harmful Algae, 8, 611-617. DOI: 10.1016/j.hal.2008.11.006

Henrichs, D.W., Olson, R.J., Sosik, H.M. & Campbell, L. (2011). Phylogenetic analysis of Brachidinium capitatum (Dinophyceae) from the Gulf of Mexico indicates membership in the Kareniaceae. Journal of Phycology, 47(2), 366-374. DOI: 10.1111/j.1529-8817.2011.00960.x

Hoagland, P., Jin, D., Polansky, L.Y., Kirkpatrick, B., Kirkpatrick, G., Fleming, L.E., Reich, A., Watkins, S.M., Ullmann, S.G. & Backer, L.C. (2009). The costs of respiratory illnesses arising from Florida gulf coast Karenia brevis blooms. Environmental Health Perspectives, 117(8), 1239–1243. DOI: 10.1289/ehp.0900645

Hoshaw, R.W. (1973). Methods for microscopic algae. Handbook of phycological methods: culture methods, 53-68.

Hulburt, E.M. (1957). The taxonomy of unarmored Dinophyceae of shallow embayments on Cape Cod, Massachusetts. The Biological Bulletin, 112, 196-219. DOI: 10.2307/1539198

Iwataki, M., Lum, W.M., Kuwata, K., Takahashi, K., Arima, D., Kuribayashi, T., Kosaka, Y., Hasegawa, N., Watanabe, T., Shikata, T., Isada, T., Orlova, T.Y. & Sakamoto, S. (2022). Morphological variation and phylogeny of Karenia selliformis (Gymnodiniales, Dinophyceae) in an intensive cold-water algal bloom in eastern Hokkaido, Japan. Harmful Algae, 114, 102204. DOI: 10.1016.j.hal.2022.102204

Kimura, B., Kamizono, M., Etoh, T., Koizumi, Y., Murakami, M. & Honjo, T. (1999). Population development of the red tide dinoflagellate Gymnodinium mikimotoi in inshore waters of Japan. Plankton Biology and Ecology, 46(1), 37-47.

Koetschan, C., Hackl, T., Müller, T., Wolf, M., Förster, F. & Schultz, J. (2012). ITS2 database IV: interactive taxon sampling for internal transcribed spacer 2 based phylogenies. Molecular Phylogenetics and Evolution, 63: 585–588.

Koizumi, Y., Uchida, T. & Honjo, T. (1996). Diurnal vertical migration of Gymnodinium mikimotoi during a red tide in Hoketsu Bay, Japan. Journal of Plankton Research, 18(2), 289-294. DOI: 10.1093/plankt/18.2.289

Kok, J.W.K. & Leong, S.C.Y. (2019). Nutrient conditions and the occurrence of a Karenia mikimotoi (Kareniaceae) bloom within East Johor Straits, Singapore. Regional Studies in Marine Science, 27, 100514. DOI: 10.1016/j.rsma.2019.100514

Kon, N.F., Lau, W.L.S., Hii, K.S., Law, I.K., Teng, S.T., Lim, H.C., Takahashi, K., Gu, H., Lim, P.T. & Leaw, C.P. (2017). Quantitative real-time PCR detection of a harmful unarmoured dinoflagellate, Karlodinium australe (Dinophyceae). Phycological Research, 65, 291-298. DOI: 10.1111/pre.12186

Krock, B., Pitcher, G., Ntuli, J. & Cembella, A. (2009). Confirmed identification of gymnodimine in oysters from the west coast of South Africa by liquid 145 chromatography-tandem mass spectrometry. African Journal of Marine Science, 31, 113-118. DOI: 10.2989/AJMS.2009.31.1.12.783

Kumar, P.S., Kumaraswami, M., Rao, G.D., Ezhilarasan, P., Sivasankar, R., Rao, V.R. & Ramu, K. (2018). Influence of nutrient fluxes on phytoplankton community and harmful algal blooms along the coastal waters of southeastern Arabian Sea. Continental Shelf Research, 161, 20-28. DOI: 10.1016/j.csr.2018.04.012

Larsen, J. & Nguyen, N.L. (2004). Potentially toxic microalgae of Vietnamese waters. Opera Botanica, 140, 5-216.

Laza-Martínez, A., David, H., Riobó, P., Miguel, I. & Orive, E. (2016). Characterization of a Strain of Fukuyoa paulensis (Dinophyceae) from the Western Mediterranean Sea. Journal of Eukaryotic Microbiology, 63(4), 481–497. DOI: 10.1111/jeu.12292

Li, X., Yan, T., Lin, J., Yu, R. & Zhou, M. (2017). Detrimental impacts of the dinoflagellate Karenia mikimotoi in Fujian coastal waters on typical marine organisms. Harmful Algae, 61, 1-12. 137. DOI: 10.1016/j.hal.2016.11.011

Li, X., Yan, T., Yu, R. & Zhou, M. (2019). A review of Karenia mikimotoi: Bloom events, physiology, toxicity and toxic mechanism. Harmful Algae, 90, 101702. DOI: 10.1016/j.hal.2019.101702

Loeblich, A. R. (1975). A seawater medium for dinoflagellates and the nutrition of Cachonina niel. Journal of Phycology, 11, 80-86. DOI: 10.1111/j.1529-8817.1975.tb02752.x

Leong, S., Yew, C., Peng, L. L., Moon, C. S., Kit, J. K. W. & Ming, S. T. L. (2015). Three new records of dinoflagellates in Singapore's coastal waters, with observations on environmental conditions associated with microalgal growth in the Johor Straits. Raffles Bulletin of Zoology, 31,24-36.

Matsuyama, Y., Uchida, T. & Honjo, T. (1999). Effects of harmful dinoflagellates, Gymnodinium mikimotoi and Heterocapsa circularisquama, red-tide on filtering rate of bivalve molluscs. Fisheries Science, 65, 248-253. DOI: 10.2331/fishsci.65.248

Merget, B., Koetschan, C., Hackl, T., Förster, F., Dandekar, T., Müller, T., Schultz, J., & Wolf, M. (2012). The ITS2 Database. Journal of Visualized Experiments, (61), 3806. DOI: 10.3791/3806

Metzger, B.P.H., Wittkopp, P.J. & Coolon, J.D. (2017). Evolutionary dynamics of regulatory changes underlying gene expression divergence among Saccharomyces species. Genome Biology and Evolution, 9(4), 843-854. DOI: 10.1093/gbe/evx035

Monaco, A. & Prouzet, P. (2015). Marine Ecosystems: Diversity and Functions. Wiley.

Müller, T., Philippi, N., Dandekar, T., Schultz, J., & Wolf, M. (2007). Distinguishing species. RNA, 13(9), 1469–1472. DOI: 10.1261/rna.617107

Nakamura, Y., Suzuki, S. & Hiromi, J. (1995). Population dynamics of heterotrophic dinoflagellates during a Gymnodinium mikimotoi red tide in the Seto Inland Sea. Marine Ecology Progress Series, 125, 269-277.

Nézan, E., Siano, R., Boulben, S., Six, C., Bilien, G., Chèze, K., Duval, A., Le Panse, S., Quéré, J. & Chomérat, 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. DOI: 10.1016/j.hal.2014.10.006

Oda M. (1935). The red tide of Gymnodinium mikimotoi n.sp. (MS.) and the effect of altering copper sulphate to prevent the growth of it. Zoological Society of Japan, 47(555): 35-48.

Ok, J.H., Jeong, H.J., Lim, A.S., Kang, H.C. You, J.H., Park, S.A. & Eom, S.H. (2023). Lack of mixotrophy in three Karenia species and the prey spectrum of Karenia mikimotoi (Gymnodiniales, Dinophyceae). Algae, 38(1), 39-55. DOI: 10.4490/algae.2023.38.2.28

Park, J., Jeong, H.J., Yoo, Y.D. & Yoon, E.Y. (2013). Mixotrophic dinoflagellate red tides in Korean waters: distribution and ecophysiology. Harmful Algae, 30, S28-S40. DOI: 10.1016/j.hal.2013.10.004

Partensky, F., Vaulot, D., Couté, A. & Sournia, A. (1988). Morphological and nuclear analysis of the bloom-forming dinoflagellates Gyrodinium cf. aureolum and Gymnodinium nagasakiense. Journal of Phycology, 24(3), 408-415. DOI: 10.1111/j.1529-8817.1988.tb04484.x

Rambaut, A. (2007). FigTree, a graphical viewer of phylogenetic trees.

Ronquist, F. & Huelsenbeck, J.P. (2003). MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics, 19, 1572-1574. DOI: 10.1093/bioninformatics/btg180

Ronquist, F., Teslenko, M., van der Mark, P., Ayres, D.L., Darling, A., Höhna, S., Larget, B., Liu, L., Suchard, M.A. & Huelsenbeck, J.P. (2012). MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology, 61, 539-542. DOI: 10.1093/sysbio/sys029

Rousset, F., Pélandakis, M. & Solignac, M. (1991). Evolution of compensatory substitutions through G-U intermediate state in Drosophila rRNA. Proceedings of the National Academy of Sciences of the United States of America, 88, 10032-10036. DOI: 10.1073/PNAS.88.22.10032.

Seibel, P.N., Müller, T., Dandekar, T., Schultz, J. & Wolf, M. (2006). 4SALE – a tool for synchronous RNA sequence and secondary structure alignment and editing. Bioinformatics, 7(498). DOI: 10.1186/1471-2105-7-498

Seibel, P.N., Müller, T., Dandekar, T. & Wolf, M. (2008). Synchronous visual analysis and editing of RNA sequence and secondary structure alignments using 4SALE. BMC Research Notes, 1(91). DOI: 10.1186/1756-0500-1-91

Seibel, P., Müller, T., Dandekar, T. & Wolf, M. (2008). Synchronous visual analysis and editing of RNA sequence and secondary structure alignments using 4SALE. BMC Research Notes, 1: 91.

Siswanto, E., Ishizaka, J., Tripathy, S.C. & Miyamura, K. (2013). Detection of harmful algal blooms of Karenia mikimotoi using MODIS measurements: a case study of Seto-Inland Sea, Japan. Remote Sensing of Environment, 129, 185-196. DOI: 10.1016/j.rse.2012.11.012

Swofford, D.L. (2003). PAUP* Phylogenetic Analysis Using Parsimony (*and Other Methods). Version 4. http://paup.csit.fsu.edu/.

Takayama, H. & Adachi, R. (1984). Gymnodinium nagasakiense sp. nov., a red-tide forming dinophyte in the adjacent waters of Japan. Bulletin of Plankton Society of Japan, 31, 7-14.

Tangen, K. (1977). Blooms of Gyrodinium aureolum (Dinophygeae) in North European waters, accompanied by mortality in marine organisms. Sarsia, 63, 123-133. DOI: 10.1080/00364827.1977.10411330

Tangen, K. & Bjornland, T. (1981). Observations on pigments and morphology of Gyrodinium aureolum Hulburt, a marine dinoflagellate contain 19’hexanoyloxyfucoxantin as the main carotenoid. Journal of Plankton Research, 3, 389-401. DOI: 10.1093/plankt/3.3.389

Tang, Y.Z., Egerton, T.A., Kong, L. & Marshall, H.G. (2008). Morphological variation and phylogenetic analysis of the dinoflagellate Gymnodinium aureolum from a tributary of Chesapeake Bay. J. Eukaryot. Microbiol. 55, 91–99. DOI: 10.1111/j.1550-7408.2008.00305.x

Teng, S.T., Lim, P.T., Lim, H.C., Rivera-Vilarelle, M., Quijano-Scheggia, S., Takata, Y., Quilliam, M.A., Wolf, M., Bates, S.S. & Leaw, C.P. (2015). A non-toxigenic but morphologically and phylogenetically distinct new species of Pseudo-nitzschia, P. sabit sp. nov. (Bacillariophyceae). Journal of Phycology, 51, 706-725. DOI: 10.1111/jpy.12318

Wang, Q., Lin, L., Chen, X., Wu, W. & Wu, H. (2022). Transportation of bloom forming species in ballast water by commercial vessels at Yangshan deep water port. Ocean and Coastal Management, 219, 106045. DOI: 10.1016/j.ocecoaman.2022.106045

Watkins, S.M.A.R., Fleming, L.E. & Hammond, R. (2008). Neurotoxic shellfish poisoning. Marine Drugs, 6, 431-455. DOI: 10.3390/md20080022

Wayne, L.R., 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, 344-355. DOI: 10.1111/j.1529-8817.2006.00305.x

Wolf, M., Achtziger, M., Schultz, J., Dandekar, T., & Müller, T. (2005). Homology modeling revealed more than 20,000 rRNA internal transcribed spacer 2 (ITS2) secondary structures. RNA, 11(11), 1616–1623. DOI: 10.1261/rna.2144205

Wolf, M., Chen S., Song, J., Ankenbrand, M., & Müller, T. (2013). Compensatory base changes in ITS2 secondary structures correlate with the biological species concept despite intragenomic variability in ITS2 sequences - a proof of concept. PLoS One, 8(6), e66726. DOI: 10.1371/journal.pone.0066726

Wolny, J.L., Whereat, E.B., Egerton, T.A., Gibala-Smith, L.A., McKay, J.R., O’Neil, M., Wazniak, C.E. & Mulholland, M.R. (2024). The occurrence of Karenia species in mid-Atlantic coastal waters:data from the Delmarva Peninsula, USA. Harmful Algae, 132, 102579. DOI: 10.1016/j.hal.2024.102579

Yanagi, T., Yamamoto, T., Koizumi, Y., Ikeda, T., Kamizono, M. & Tamori, H. (1995). A numerical simulation of red tide formation. Journal of Marine Systems, 6, 269-285. DOI: 10.1016/0924-7963(94)00030-K

Yñiguez, A.T., Lim, P.T., Leaw, C.P., Jipanin, S.J., Iwataki, M., Benico, G. & Azanza, R.V. (2021). Over 30 years of HABs in the Philippines and Malaysia: what have we learned? Harmful Algae, 102, 101776. DOI: 10.1016/j.hal.2021.101776

Yuan, J., Mi, T., Zhen, Y., & Yu, Z. (2012). Development of a rapid detection and quantification method of Karenia mikimotoi by real-time quantitative PCR. Harmful Algae, 17, 83-91.DOI: 10.1016/J.HAL.2012.03.004

Zhang, W., Zhang, Q., Smith, K.F., Qiu, L., Liu, C., Yin, X. & Liu, Q. (2022). Development of specific DNA barcodes for the Dinophyceae family Kareniaceae and their application in the South China Sea. Frontiers in Marine Science, 9. DOI: 10.3389/fmars.2022.851605

Zhang, Y., Song, X. & Zhang, P. (2023). Combined effects of toxic Karenia mikimotoi and hypoxia on the juvenile abalone Haliotis discus hannai. Journal of Shellfish Research, 42(2), 373-379. DOI: 10.2983/035.042.0207

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2024-12-23

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ANDREW CHIBA, S. U., TENG, S. T., MOHAMAD, S., ABDULLAH, N., LAW, I. K., LIM, P. T., & LEAW, C. P. (2024). Morphology and Molecular Characterisation of Karenia mikimotoi (Dinophyceae) from Sabah Malaysian Borneo, with a Focus on the Second Internal Transcribed Spacer (ITS2) of Ribosomal RNA gene : Characterisation of Karenia mikimotoi from Sabah. Borneo Journal of Resource Science and Technology, 14(2), 81–97. https://doi.org/10.33736/bjrst.7417.2024