Harmful non-indigenous dinoflagellate cysts in China: A review
Keywords:
biological invasion, metabarcoding, molecular identification, morphological identificationAbstract
Harmful dinoflagellate cysts (e.g. dinocysts) represent a great threat to marine and coastal ecosystems and even human health. As dinocysts have resistant cell walls that allow dinoflagellate species to successfully survive harsh environments, they can easily pass through multiple barriers during biological invasions and successfully colonize new locations. In introduced ranges, dinocysts often serve as seeds for harmful algal blooms, which can result in large-scale environmental disasters and economic losses. Correct identification of dinocysts represents the first step for both ecological studies and management programs. However, traditional methods, which are based on morphological observations, pose great technical challenges for dinocysts. Recent advances in molecular techniques, such as high-throughput sequencing-based metabarcoding, have tremendously revolutionized our abilities to detect marine biodiversity. Here, we summarize species composition of non-indigenous/cryptogenic dinocysts and their identification methods commonly used in China, discuss major problems in traditional morphological identification and technical issues of molecular identification, and finally propose future perspectives for the efficient identification of non-indigenous dinocysts using high-throughput sequencing-based metabarcoding. We also discuss technical issues that should be addressed before high-throughput sequencing-based metabarcoding can be widely used for dinocyst identification at large geographical scales.
References
Anderson, D.M., Wall, D., 1978. Potential importance of benthic cysts of Gonyaulax tamarensis and Gonyaulax excavata in initiating toxic dinoflagellate blooms. J. Phycol. 14(2), 224–234.
Anderson, D.M., Stock, C.A., Keafer, B.A., Bronzino, N.A., Thompson, B., McGillicuddy, D.J., Keller, M., Matrai, P.A., Martin. J., 2005. Alexandrium fundyense cyst dynamics in the Gulf of Maine: Long-term time series of abundance and distribution, and linkages to past and future blooms. Deep-Sea Res. Pt. II. 52(19–21), 2522–2542.
Balech, E. (Ed.) 1995. The genus Alexandrium Halim (Dinoflagellate) Sherkin Island Marine Station Publicaiton, Sherkin Island, Co. Cork,
Ireland.
Bates, S.S., Trainer, V.L., 2006. The ecology of harmful diatoms. In: Granéli, E., Turner, J. T. (Eds.), Ecology of harmful algae Springer-Verlag, Heidelberg.
Bravo, I., Figueroa, R.I., 2014. Towards an ecological understanding of dinoflagellate cyst functions. Microorganisms 2(1), 11–32.
Brown, E.A., Chain, F.J., Zhan, A., MacIsaac, H.J., Cristescu, M.E., 2016. Early detection of aquatic invaders using metabarcoding reveals a high number of non-indigenous species in Canadian ports. Diversity Distrib 22(10), 1045–1059.
Campbell, K., Rawn, D.F., Niedzwiadek, B., Elliott, C.T., 2011. Paralytic shellfish poisoning (PSP) toxin binders for optical biosensor technology: problems and possibilities for the future: a review. Food Addit. Contam. 28(6), 711–725.
Casas-Monroy, O., Roy, S., Rochon, A., 2011. Ballast sediment-mediated transport of non-indigenous species of dinoflagellates on the East Coast of Canada. Aquatic Invasions 6(3), 231–248.
Dai, X.F., Lu, D.D., Xia, P., Wang, H.X., He, P.X., 2012. A 50-year temporal record of dinoflagellate cysts in sediments from the Changjiang estuary, East China Sea, in relation to climate and catchment changes. Estuar. Coast. Shelf Sci. 112, 192–197.
Gómez, F., 2012. A quantitative review of the lifestyle, habitat and trophic diversity of dinoflagellates (Dinoflagellata, Alveolata). Syst. Biodivers. 10(3), 267–275.
Gu, H.F., 2007. Resting cysts, life cycle and phylogenetic analysis of typical algae from Southeastern China Sea. PhD dissertation, Ocean University of China, Shandong.
Gu, H.F., Wang, Y., 2007. The first record of Ensiculifera Balech and Fragilidium Balech (Dinophyceae) from Chinese coast. Acta Phytotaxonomica Sinica 45(6), 828–840.
Gu, H.F., Fang, Q., Li, R.X., Lan, D.Z., Zhu, M.Y., 2004. Preliminary study on dinoflagellate cysts in Changjiang River esturary. Oceanologia Et Limnologia Sinica 35, 413–423.
Gu, H.F., Zeng, N., Liu, T.T., Yang, W.D., Muller, A., Krock, B., 2013a. Morphology, toxicity, and phylogeny of Alexandrium (Dinophyceae) species along the coast of China. Harmful Algae 27(7), 68–81.
Gu, H.F., Zeng, N., Xie, Z.X., Wang, D.Z., Wang, W.G., Yang, W.D., 2013b. Morphology, phylogeny, and toxicity of Atama complex (Dinophyceae) from the Chukchi Sea. Polar Biol 36(3), 427–436.
Gu, H., Liu, T., Vale, P., Luo, Z., 2013c. Morphology, phylogeny and toxin profiles of Gymnodinium inusitatum, sp. nov. Gymnodinium catenatum, and Gymnodinium microreticulatum, (Dinophyceae) from the Yellow Sea, China. Harmful Algae 28(28), 97–107.
Head, M.J., 1994. Morphology and paleoenvironmental significance of the Cenozonic dinoflagellate genera Tectatodinium and Habibacysta. Micropaleontology 40(4), 289–321.
Iwataki, M., Kawami, H., Mizushima, K., Mikulski, C. M., Doucette, G. J., Relox, J. R., Matsuoka, K., 2008. Phylogenetic relationships in the harmful dinoflagellate Cochlodinium polykrikoides (Gymnodiniales, Dinophyceae) inferred from LSU rDNA sequences. Harmful Algae 7(3), 271–277.
John, U., Litaker, R.W., Montresor, M., Murray, S., Brosnahan, M.L, Anderson, D.M., 2014. Formal revision of the Alexandrium tamarense species complex (Dinophyceae) taxonomy: the introduction of five species with emphasis on molecular-based (rDNA) classification. Protist 165(6), 779–804.
Kamikawa, R., Nagai, S., Hosoi-Tanabe, S., Itakura, S., Yamaguchi, M., Uchida, Y., Baba, T., Sako, Y., 2007. Application of real-time PCR assay for detection and quantification of Alexandrium tamarense and Alexandrium catenella cysts from marine sediments. Harmful Algae 6(3), 413–420.
Ki, J.S., 2012. Hypervariable regions (V1-V9) of the dinoflagellate 18S rDNA using a large dataset for marker considerations. J. Appl. Phycol. 24, 1035–1043.
Kremp, A., Tahvanainen, P., Litaker, W., Krock, B., Suikkanen, S., Leaw, C.P., Tomas, C., 2014. Phylogenetic relationships, morphological variation, and toxin patterns in the Alexandrium ostenfeldii (Dinophyceae) complex: implications for species boundaries and identities. J. Phycol. 50(1), 81–100.
Kohli, G.S., Neilan, B.A., Brown, M.V., Hoppenrath, M., Murray, S.A., 2014. Cob gene pyrosequencing enables characterization of benthic dinoflagellate diversity and biogeography. Environ. Microbiol. 16, 467–485.
Lim, C.S., Leong, Y.L., Tan, K.S., 2016. Managing the risk of non-indigenous marine species transfer in Singapore using a study of vessel movement. Mar. Pollut. Bull. 115, 332–344.
Lin, S., Zhang, H., Hou, Y., Miranda, L., Bhattacharya, D., 2006. Development of a dinoflagellate-oriented PCR primer set leads to detection of picoplanktonic dinoflagellates from Long Island Sound. Applied Environ. Microb. 72(8), 5626–5630.
Lin, S., Zhang, H., Hou, Y., Zhuang, Y., Miranda, L., 2009. High-level diversity of dinoflagellates in the natural environment, revealed by assessment of mitochondrial cox1 and cob genes for dinoflagellate DNA barcoding. Appl. Environ. Microb. 75(5), 1279–1290.
Lin, S., Wang, L., Zheng, L.M., Dong, Y.W., Liu, S.F., Ding, S.X., Ye, N.H., Cao, W.Q., Zhuang, Z.M., 2014. Current status and future prospect of DNA barcoding in marine biology. Acta Oceanol. Sin. 36, 1–17.
Matsuoka, K., Fukuyo, Y., 2000. Technical guide for modern dinoflagellate cyst study WESTPAC-HAB Japanese Society for the Promotion of Science,
Japan.
Mertens, K.N., Wolny, J., Carbonell-Moore, C., Bogus, K., Ellegaard, M., Limoges, A., Vernal, A.D., Gurdebeke, P., Omura, K., Abdulrahman, A.M., 2015. Taxonomic re-examination of the toxic armored dinoflagellate Pyrodinium bahamense Plate 1906: Can morphology or LSU sequencing separate P. bahamense var. compressum from var. bahamense. Harmful Algae 41, 1–24.
Morado, J.F., Jensen, P., Hauzer, L., Lowe, V., Califf, K., Roberson, N., Shavey, C., Woodby, D., 2005. Species identity and life history of Hematodinium, the causitive agent of bitter crab syndrome in north east pacific snow, Chionoecetes opilio, and tanner, C. bairdi, crabs, Anchorage, AK, USA: North Pacific Research Board.
Nagai, S., Miyamoto, S., Ino, K., Tajimi, S., Nishi, H., Tomono, J., 2015. Easy detection of multiple Alexandrium species using DNA chromatography chip. Harmful Algae 51, 97–106.
Penna, A., Battocchi, C., Garcés, E., Anglès, S., Cucchiari, E., Totti, C., Kremp, A., Satta, C., Giacobbe, M.G., Bravo, I., 2010. Detection of microalgal resting cysts in European coastal sediments using a PCR-based assay. Deep-Sea Res. Pt. II. 57(S3–4), 288–300.
Stern, R.F., Andersen, R.A., Jameson, I., Küpper, F.C., Coffroth, M.A., Vaulot, D., Gall, F.L., Veron, B., Brand, J.J., Skelton, H., Kasai, F., Lilly, E.L., Keeling, P.J., 2012. Evaluating the ribosomal internal transcribed spacer (ITS) as a candidate dinoflagellate barcode marker. PLoS One 7(8), e42780.
Sun, M.Q., 2005. The study of exotic dinoflagellate in sea area round Xiamen Island. Ph.D. dissertation, Xiamen University, Xiamen, China.
Wang, Y., 1980. The coast of China. Geosci. Can. 7(3), 109–113.
Wang, Z.H. (Ed.), 2007. Study on dinoflagellate cysts and red tide along the coast of China Ocean Press, Beijing, China.
Wang, Z.H., Kang, W., 2014. Distribution of dinocysts and germination of phytoplankton resting spores in surface sediments form Zhelin Bay, the South China Sea. Acta Scientiae Circumstantiae 34, 2043–2050.
Wang, Z.H., Fu, Y.H., Kang, W., Liang, J.F., Gu, Y.G., Jiang, X.L., 2013. Germination of phytoplankton resting cells from surface sediments in two areas of the Southern Chinese coastal waters. Mar. Ecol. 34(2), 218–232.
Xiong, W., Li, H., Zhan, A., 2016. Early detection of invasive species in marine ecosystems using high-throughput sequencing: technical challenges and possible solutions. Mar. Biol. 163(6), 139.
Zhan, A., MacIsaac, H.J., 2015. Rare biosphere exploration using high-throughput sequencing: research progress and perspectives. Conserv. Genet. 16(3), 513–522.
Zhan, A., Hulák, M., Sylvester, F., Huang, X., Adebayo, A.A., Abbott, C.L., Adamowicz, S.J., Heath, D.D., Cristescu, M.E., MacIsaac, H.J., 2013. High sensitivity of 454 pyrosequencing for detection of rare species in aquatic communities. Methods Ecol. Evol. 4, 558–565.
Zhan, A., Bailey, S.A., Heath, D.D., MacIsaac, H.J., 2014. Performance comparison of genetic markers for high-throughput sequencing based biodiversity assessment in complex communities. Mol. Ecol. Resour. 14, 1049–1059.
Zhang, F., Dickman, M., 1999. Mid-ocean exchange of container vessel ballast water. 1: Seasonal factors affecting the transport of harmful diatoms and dinoflagellates. Mar. Ecol. Prog. Ser. 176, 243–251.
Zhang, C.Y., Chen, G.F., Cai, P.P., Wang, Y.Y., Guo, C.L., 2015. Development and evaluation of a reverse dot blot assay for the simultaneous detection of common toxic microalgae along the Chinese coast. Harmful Algae 47, 86–96.
Zonneveld, K.A., Pospelova, V., 2015. A determination key for modern dinoflagellate cysts. Palynology 39(3), 387–409.
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