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Dinoflagellate Tripos species composition and seasonal dynamics in Jiaozhou Bay revealed through 18S rDNA V4-based metabarcoding analysis

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Abstract

Tripos is one of the largest dinoflagellate genera with ~800 reported taxa widely distributed in global marine ecosystems. These diverse Tripos species are ecologically important as critical primary producers and some Tripos species are also harmful algal bloom (HAB) species that may pose significant negative impact on marine ecosystems. However, due to the high morphological intraspecific variability and plasticity of numerous Tripos species, morphology-based identification and tracking of their dynamic changes have been both technically challenging and inconclusive. In this project, we carried out metabarcoding analysis of Tripos species in Jiaozhou Bay (JZB) through amplifying and sequencing of the common molecular marker 18S rDNA V4. The analysis identified five Tripos species (T. furca, T. fusus, T. eugrammus, T. falcatus and T. massiliensis), including two (T. eugrammus and T. falcatus) identified for the first time in JZB, demonstrating the competitive strength of metabarcoding analysis. This analysis of time-series samples collected in JZB revealed interesting seasonal dynamic changes of Tripos species, with different species demonstrating differential seasonal preferences. This analysis also suggested the possible existence of 11 additional Tripos species in JZB. The inconclusive identification of these 11 potential Tripos species indicated that the resolution of the common molecular marker 18S rDNA V4 applied in this study is inadequate and that the molecular reference data for Tripos is still limited. Selection of molecular markers with higher resolution (such as 28S rDNA D1-6) and the completion of reference sequences of Tripos species may facilitate more accurate identification of and tracking of their dynamic changes.

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Data availability

The sequencing results (raw data) have been submitted to NCBI, and the BioProject numbers are PRJNA577777 and PRJNA733859.

References

  • Al Gheilani HM, Matsuoka K, AlKindi AY, Amer S, Waring C (2011) Fish kill incidents and harmful algal blooms in Omani Waters. J Ag Mar Sci 16:23–33

    Google Scholar 

  • Anderson D (1995) ECOHAB, the ecology and oceanography of harmful algal blooms: a national research agenda. Woods Hole Oceanographic Institution, Woods Hole, MA, p 66

  • Anderson MP, Davies CH, Eriksen RS (2022) Latitudinal variation, and potential ecological indicator species, in the dinoflagellate genus Tripos along 110° E in the south-east Indian Ocean. Deep Sea Res II 203:105–150

    Article  Google Scholar 

  • Archangi B, Savari A, Nabavi SMB (2023) Combined morphological and molecular phylogenetic analysis of the genus Tripos (Dinophyceae) from the Persian Gulf. J Phycol Res 7:969–987

    Google Scholar 

  • Baek SH, Shimode S, Kikuchi T (2006) Reproductive ecology of dominant dinoflagellate, Ceratium furca, in the coastal area of Sagami Bay. Coastal Mar Sci 30:344–352

    Google Scholar 

  • Baek SH, Shimode S, Kikuchi T (2007) Reproductive ecology of the dominant dinoflagellate, Ceratium fusus, in coastal area of Sagami Bay, Japan. J Oceanogr 63:35–45

    Article  Google Scholar 

  • Baek SH, Shimode S, Han M-S, Kikuchi T (2008) Population development of the dinoflagellates Ceratium furca and Ceratium fusus during spring and early summer in Iwa Harbor, Sagami Bay, Japan. Ocean Sci J 43:49–59

    Article  Google Scholar 

  • Bockstahler KR, Coats DW (1993) Spatial and temporal aspects of mixotrophy in Chesapeake Bay dinoflagellates. J Eukaryot Microbiol 40:49–60

    Article  Google Scholar 

  • Callahan BJ, Grinevich D, Thakur S, Balamotis MA, Yehezkel TB (2021) Ultra-accurate microbial amplicon sequencing with synthetic long reads. Microbiome 9:130

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Callahan BJ, McMurdie PJ, Holmes SP (2017) Exact sequence variants should replace operational taxonomic units in marker-gene data analysis. ISME J 11:2639–2643

    Article  PubMed  PubMed Central  Google Scholar 

  • Callahan BJ, P.J. M, Rosen MJ, Han AW, Johnson AJ, Holmes SP, (2016) DADA2: High-resolution sample inference from lllumina amplicon data. Nat Methods 13:581–583

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Castaño C, Berlin A, Brandström Durling M, Ihrmark K, Lindahl BD, Stenlid J, Clemmensen KE, Olson Å (2020) Optimized metabarcoding with Pacific biosciences enables semi-quantitative analysis of fungal communities. New Phytol 228:1149–1158

    Article  Google Scholar 

  • Chen N, Chen Y (2021) Advances in the study of biodiversity of phytoplankton and red tide species in China (II): the East China Sea. Oceanol Limnol Sinica 52:363–384

    CAS  Google Scholar 

  • Chen N, Cui Z, Xu Q (2021) Advances in the study of biodiversity of phytoplankton and red tide species in China (IV): the Changjiang Estuary. Oceanol Limnol Sinica 52:402–417

    Google Scholar 

  • Chen N, Huang H (2021) Advances in the study of biodiversity of phytoplankton and red tide species in China (I): the Bohai Sea. Oceanol Limnol Sinica 52:346–362

    Google Scholar 

  • Chen N, Zhang M (2021) Advances in the study of biodiversity of phytoplankton and red tide species in China (III): the South China Sea. Oceanol Limnol Sinica 52:385–401

    Google Scholar 

  • Chen N, Zhang M, Liu S, Cui Z (2023) Diversity of HAB species in coastal regions of China. Oceanol Limnol Sinica 54:599–624

    Google Scholar 

  • Chitari RR, Anil AC, Kulkarni VV, Narale DD, Patil JS (2017) Inter- and intra-annual variations in the population of Tripos from the Bay of Bengal. Curr Sci 112:1219–1229

    Article  Google Scholar 

  • Dodge JD, Marshall HG (1994) Biogeographic analysis of the armored planktonic dinoflagellate Ceratium in the north atlantic and adjacent seas. J Phycol 30:905–922

    Article  Google Scholar 

  • Edoa FDO, Takem GE, Medjo PB, Mama AC, Zambo GB, Kueppo JÉK, Mahamat TS, Togouet SHZ (2022) Spatio-temporal variation of dinoflagellates of the genera Ceratium (Schrank 1793) and Protoperidinium (Bergh 1881) in relationship with some abiotic variables in the Atlantic coast of Kribi (South Region-Cameroon). Open J Mar Sci 12:161–184

    Article  Google Scholar 

  • Elbrachter M (1973) Population dynamics of Ceratium in coastal waters of the Kiel Bay. Oikos 15:43–48

    Google Scholar 

  • Gómez F (2013) Reinstatement of the dinoflagellate genus Tripos to replace Neoceratium, marine species of Ceratium (Dinophyceae, Alveolata). Cicimar Oceánides 28:1–22

    Article  Google Scholar 

  • Gómez F (2021) Speciation and infrageneric classification in the planktonic dinoflagellate Tripos (Gonyaulacales, Dinophyceae). Current Chinese Science 1:346–372

    Article  Google Scholar 

  • Gómez F, Moreira D, López-García P (2010) Neoceratium gen. nov., a new genus for all marine species currently assigned to Ceratium (Dinophyceae). Protist 161:35–54

    Article  PubMed  Google Scholar 

  • Graham HW (1941) An oceanographic consideration of the dinoflagellate genus Ceratium. Ecol Monogr 11:99–116

    Article  CAS  Google Scholar 

  • Guillou L, Bachar D, Audic S, Bass D, Berney C, Bittner L, Boutte C, Burgaud G, de Vargas C, Decelle J, del Campo J, Dolan JR, Dunthorn M, Edvardsen B, Holzmann M, Kooistra WHCF, Lara E, Le Bescot N, Logares R, Mahé F, Massana R, Montresor M, Morard R, Not F, Pawlowski J, Probert I, Sauvadet A-L, Siano R, Stoeck T, Vaulot D, Zimmermann P, Christen R (2013) The Protist Ribosomal Reference database (PR2): a catalog of unicellular eukaryote Small Sub-Unit rRNA sequences with curated taxonomy. Nucl Acids Res 41:D597–D604

    Article  CAS  PubMed  Google Scholar 

  • Guo S, Sun J, Dai M, Liu Z (2012) Phytoplankton assemblages in East China Sea in winter 2009. Acta Ecol Sinica 32:3266–3278

    Article  Google Scholar 

  • Guo S, Zhu M, Zhao Z, Liang J, Zhao Y, Du J, Sun X (2019) Spatial-temporal variation of phytoplankton community structure in Jiaozhou Bay. China. J Oceanol Limnol 37:1611–1624

    Article  CAS  Google Scholar 

  • Hallegraeff G, Eriksen R, Davies C, Slotwinski A, McEnnulty F, Coman F, Uribe-Palomino J, Tonks M, Richardson A (2020) The marine planktonic dinoflagellate Tripos: 60 years of species-level distributions in Australian waters. Aust Systemat Bot 33:392–411

    Google Scholar 

  • He L, Yu Z, Xu X, Zhu J, Yuan Y, Cao X, Song X (2023) Metabarcoding analysis identifies high diversity of harmful algal bloom species in the coastal waters of the Beibu Gulf. Ecol Evol 13:e10127

  • Holligan P, Harbour D (1977) The vertical distribution and succession of phytoplankton in the western English Channel in 1975 and 1976. J Mar Biol Assoc U K 57:1075–1093

    Article  CAS  Google Scholar 

  • Horner RA, Garrison DL, Plumley FG (1997) Harmful algal blooms and red tide problems on the U.S. west coast. Limnol Oceanogr 42:1076–1088

    Article  Google Scholar 

  • Jerney J, Hällfors H, Jakobsen H, Jurgensone I, Karlson B, Kremp A, Lehtinen S, Majaneva M, Meissner C, Norros V, Sildever S, Suikkanen S, Teeveer K (2023) DNA metabarcoding - Guidelines to monitor phytoplankton diversity and distribution in marine and brackish waters. Nordic Co-operation | Nordic Council & Nordic Council of Ministers, Copenhagen: Nordisk Ministerråd

  • Kolde R (2019) R (2019) pheatmap: Pretty Heatmaps. R package version 1.0.12. https://CRAN.R-project.org/package=pheatmap. Accessed 10 Jan 2024

  • Kudela RM, Berdalet E, Enevoldsen H, Pitcher G, Raine R, Urban E (2017) GEOHAB: The Global Ecology and Oceanography of Harmful Algal Blooms program motivation, goals, and legacy. Oceanography 30:12–21

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lee J, An S, Chung H, Shah MMR (2014) New records of genus Tripos (Dinophyceae) around Jeju Island. Korea. J Ecol Env 37:271–284

    Article  Google Scholar 

  • Leigh JW, Bryant D (2015) POPART: full-feature software for haplotype network construction. Meth Ecol Evol 6:1110–1116

    Article  Google Scholar 

  • Li A, Stoecker D, Coats DW, Adam EJ (1996) Ingestion of fluorescently labeled and phycoerythrin-containing prey by mixotrophic dinoflagellates. Aquat Microb Ecol 10:139–147

    Article  Google Scholar 

  • 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. Appl Environ Microbiol 72(8):5626–5630

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu S, Chen N (2021) Advances in biodiversity analysis of phytoplankton and harmful algal bloom species in the Jiaozhou Bay. Mar Sci 45:170–188

    Google Scholar 

  • Liu S, Cui Z, Zhao Y, Chen N (2022) Composition and spatial-temporal dynamics of phytoplankton community shaped by environmental selection and interactions in the Jiaozhou Bay. Water Res 218:118488

  • Lyakh A, Bryantseva Y (2014) Seasonal polymorphism of the Black Seas dinoflagellates from genus Ceratium: C. furca, C. fusus, C. tripos (Dinophyceae). Modern Phytomorphology 5:209–214

    Google Scholar 

  • Machida M, Fujitomi M, Hasegawa K, Kudo T, Kai M, Kobayashi T, Uede T (1999) Red tide of Ceratium furca along the Pacific coast of central Japan in 1997. Nippon Suisan Gakkaishi 65:755–756

    Article  Google Scholar 

  • Martin M (2011) Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet J 17:10–12

    Article  Google Scholar 

  • Matrai PA (1986) The distribution of the dinoflagellate Ceratium in relation to environmental factors along 28 °N in the eastern North Pacific. J Plankton Res 8:105–118

    Article  Google Scholar 

  • Mitra A, Flynn KJ, Tillmann U, Raven JA, Caron D, Stoecker DK, Not F, Hansen PJ, Hallegraeff G, Sanders R (2016) Defining planktonic protist functional groups on mechanisms for energy and nutrient acquisition: incorporation of diverse mixotrophic strategies. Protist 167:106–120

    Article  CAS  PubMed  Google Scholar 

  • Moreira RA, Rocha O, Santos R, Laudares-Silva R, Dias ES, Eskinazi-Sant’Anna E (2015) First record of Ceratium furcoides (Dinophyta), an invasive species, in a temporary high-altitude lake in the Iron Quadrangle (MG, Southeast Brazil). Braz J Biol 75:98–103

    Article  CAS  PubMed  Google Scholar 

  • Morton SL, Shuler A, Paternoster J, Fanolua S, Vargo D (2011) Coastal eutrophication, land use changes and Ceratium furca (Dinophyceae) blooms in Pago Pago Harbor, American Samoa 2007–2009. Chin J Oceanol Limnol 29:790–794

    Article  Google Scholar 

  • Mulford RA (1963) Distribution of the dinoflagellate genus Ceratium in the tidal and offshore waters of Virginia. Chesapeake Sci 4:84–89

    Article  Google Scholar 

  • Nielsen TG (1991) Contribution of zooplankton grazing to the decline of a Ceratium bloom. Limnol Oceanogr 36:1091–1106

    Article  Google Scholar 

  • Nordli E (1957) Experimental studies on the ecology of Ceratia. Oikos 8:200–265

    Article  Google Scholar 

  • Okolodkov YB (2010) Ceratium Schrank (Dinophyceae) of the national park Sistema Arrecifal Veracruzano, Gulf of Mexico, with a key for identification. Acta Botánica Mexicana 93:41–101

    Article  Google Scholar 

  • Orellana-Cepeda E, Granados-Machuca C, Serrano-Esquer J (2004) Ceratium furca: one posible cause of mortality of cultured blue-fin Tuna at Baja California, Mexico. In: Steidinger KA, Lansberg JH, tomas CR, Vargo GA (eds) Harmful Algae 2002. Florida and Wildlife Conservation Commission, Florida Institute of Oceanography and Intergoverment Oceanographic Commission of UNESCO, pp 514–516

  • Pawlowski J, Apothéloz‐Perret‐Gentil L, Mächler E, Altermatt F (2020) Environmental DNA applications for biomonitoring and bioassessment in aquatic ecosystems: guidelines. Federal Office for the Environment (FOEN/BAFU), Bern. Environ Stud 2010:71

  • Pitcher GC, Probyn TA (2011) Anoxia in southern Benguela during the autumn of 2009 and its linkage to a bloom of the dinoflagellate Ceratium balechii. Harmful Algae 11:23–32

    Article  Google Scholar 

  • Qian S, Wang X, Chen G (1983) The phytoplankton of the Jiaozhou Bay. Department of Marine Biology 13(1):39-56

  • Qiao L, Liang S, Song D, Wu W, Wang XH (2019) Jiaozhou Bay. In: Wang XH (ed) Sediment Dynamics of Chinese Muddy Coasts and Estuaries. Academic Press, London, pp 5–23

    Google Scholar 

  • Revelle WR (2017) psych: Procedures for personality and psychological research. Northwestern University, Evanston, IL, USA, Version = 2.4.3. Available at: https://CRAN.R-project.org/package=psych

  • Saunders GW, Hill DRA, Sexton JP, Andersen RA (1997) Small-subunit ribosomal RNA sequences from selected dinoflagellates: testing classical evolutionary hypotheses with molecular systematic methods. In: Bhattacharya D (ed) Origins of Algae and their Plastids. Springer, Vienna, pp 237–259

    Chapter  Google Scholar 

  • Shannon P, Markiel A, Ozier O, Baliga N, Wang J, Ramage D, Amin N, Schwikowski B, Ideker T (2003) Cytoscape: a software Environment for integrated models of biomolecular interaction networks. Genome Res 13:2498–2504

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shen Z, Yao Y, Wu Y (2016) Silica supply and diatom blooms in the Jiaozhou Bay, China. Acta Oceanol Sinica 35:20–27

    Article  CAS  Google Scholar 

  • Smalley GW, Coats DW (2002) Ecology of the red-tide dinoflagellate Ceratium furca: distribution, mixotrophy, and grazing impact on ciliate populations of Chesapeake Bay. J Eukaryot Microbiol 49:63–73

    Article  PubMed  Google Scholar 

  • Smalley GW, Coats DW, Adam EJ (1999) A new method using fluorescent microspheres to determine grazing on ciliates by the mixotrophic dinoflagellate Ceratium furca. Aquat Microb Ecol 17:167–179

    Article  Google Scholar 

  • Sournia A (1967) Le genre Ceratium (Pe´ridinien planctonique) dans Le Canal Du Mozambique. Contribution a`une re´vision mondiale. Vie Milieu A 18:375–440

    Google Scholar 

  • Sournia A (1986) Atlas du Phytoplancton marin. Vol. 1: Cyanophycées, Dictyophycées, Raphidophycées. Editions du CNRS, Paris, p 219

  • Stoeck T, Bass D, Nebel M, Christen R, Jones MD, Breiner HW, Richards TA (2010) Multiple marker parallel tag environmental DNA sequencing reveals a highly complex eukaryotic community in marine anoxic water. Molec Ecol 19:21–31

    Article  CAS  Google Scholar 

  • Stoecker DK (1998) Conceptual models of mixotrophy in planktonic protists and some ecological and evolutionary implications. Eur J Protistol 34:281–290

    Article  Google Scholar 

  • Taberlet P, Coissac E, Pompanon F, Brochmann C, Willerslev E (2012) Towards next-generation biodiversity assessment using DNA metabarcoding. Mol Ecol 21:2045–2050

    Article  CAS  PubMed  Google Scholar 

  • Taylor FJR (1966) Phytoplankton of the south western Indian Ocean. Nova Hedwigia 12:433–476

    Google Scholar 

  • Taylor FJR (1976) Dinoflagellates from the International Indian Ocean Expedition. A material collected by the RV" Anton Bruun" 1963–1964. Bibl Bot 132:1–234

    Google Scholar 

  • Tunin-Ley A, Labat J-P, Gasparini S, Mousseau L, Lemée R (2007) Annual cycle and diversity of species and infraspecific taxa of Ceratium (Dinophyceae) in the Ligurian Sea, northwest Mediterranean. J Phycol 43:1149–1163

    Article  Google Scholar 

  • Tunin-Ley A, Fdr Ibañez, Labat J-P, Zingone A, Lémée R (2009) Phytoplankton biodiversity and NW Mediterranean Sea warming: changes in the dinoflagellate genus Ceratium in the 20th century. Mar Ecol Prog Ser 375:85–99

    Article  Google Scholar 

  • Wei T, Simko V (2017) R package "corrplot": Visualization of a Correlation Matrix (Version 0.84). https://github.com/taiyun/corrplot. Accessed 23 Dec 2023

  • Weiler C (1980) Population structure and in situ division rates of Ceratium in oligotrophic waters of the North Pacific central gyre. Limnol Oceanogr 25:610–619

    Article  Google Scholar 

  • Wood EJF (1964) Studies in microbial ecology of the Australasian region. Nova Hedwigia Beih 8:5–54

    Google Scholar 

  • Yao Y, Chen N (2021) Biodiversity of phytoplankton and red tide species in the Pearl River estuary. Mar Sci 45:75–90

    Google Scholar 

  • Zingone A, Enevoldsen HO (2000) The diversity of harmful algal blooms: a challenge for science and management. Ocean Coast Manage 43:725–748

    Article  Google Scholar 

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Acknowledgements

We are grateful to colleagues from the Jiaozhou Bay Marine Ecosystem Research Station for the opportunity to participate in the investigation expeditions. Statistical analyses were supported by Oceanographic Data Center, IOCAS.

Funding

This research was supported by the Natural Science Foundation of China (42176162), the National Key Research and Development (R&D) Program of China (grant No.2022YFC3105200), the Marine S&T Fund of Shandong Province for Pilot National Laboratory for Marine Science and Technology (Qingdao) (LSKJ202203700), the Strategic Priority Research Program of Chinese Academy of Sciences (XDB42000000), the Chinese Academy of Sciences Pioneer Hundred Talents Program (to Nansheng Chen), the Taishan Scholar Project Special Fund (to Nansheng Chen).

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Nansheng Chen contributed to the study conception and design. XianliangHuang, Kuiyan Liu performed metabarcoding analyses. Shuya Liu, Zongmei Cui, Xiangxiang Ding and Yongfang Zhao carried out sample collection. Xianliang Huang wrote the first draft of the manuscript. All authors read and approved the final manuscript.

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Correspondence to Nansheng Chen.

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Huang, X., Liu, K., Ding, X. et al. Dinoflagellate Tripos species composition and seasonal dynamics in Jiaozhou Bay revealed through 18S rDNA V4-based metabarcoding analysis. J Appl Phycol (2024). https://doi.org/10.1007/s10811-024-03239-5

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