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De novo transcriptome of the newly described phototrophic dinoflagellate Yihiella yeosuensis: comparison between vegetative cells and cysts

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Abstract

Dinoflagellates are often responsible for red tides or harmful algal blooms. Many dinoflagellates move quickly to capture prey cells, escape from predation, and conduct diurnal vertical migrations, but they form cysts (non-motile stage) when growth conditions are not favorable. To investigate differences in gene expression between vegetative cells and cysts of dinoflagellates, transcriptomes of the newly described dinoflagellate Yihiella yeosuensis, one of the fastest dinoflagellates, at the cysts and vegetative cells were de novo assembled. The gene expression profiles of Y. yeosuensis showed 5479 up-regulated and 4790 down-regulated significantly differentially expressed genes, when cells changed from the vegetative cells to cysts. In particular, ‘polyketide synthase’ and ‘cell-wall biogenesis’ genes, related to anti-predation, were highly up-regulated, whereas flagellum-related genes, related to motility, were generally down-regulated. Among the flagellum-related genes of Y. yeosuensis, the ‘central pair’ and ‘radial spoke’ genes, related to direct flagellar movement, were most down-regulated genes. When approximately a hundred flagellum-related genes of motile and non-motile microalgae and plants were analyzed, the number of the genes increased with increasing motility, and furthermore, there was a considerable difference in the presence of the ‘central pair’ and ‘radial spoke’ genes among the motile microalgae. Therefore, high down-regulation of the ‘central pair’ and ‘radial spoke’ genes when Y. yeosuensis cells change from the motile to non-motile stage is possibly related to the presence of these genes in microalgae and plants in their evolution. Conclusively, when Y. yeosuensis form cysts, motility might trade off with anti-predation.

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Data accessibility

All data belong to BioProject PRJNA517580; BioSample SAMN10837594 and SAMN10837533. The illumina sequenced read data reported in this article have been deposited in the NCBI Sequence Read Archive (SRA Accession number: SRR8505364-SRR8505369).

References

  • Akbar MA, Ahmad A, Usup G, Bunawan H (2018) RNA-Seq as an emerging tool for marine dinoflagellate transcriptome analysis: process and challenges. Processes 6(1):5

    Google Scholar 

  • Alavi M, Miller T, Erlandson K, Schneider R, Belas R (2001) Bacterial community associated with Pfiesteria-like dinoflagellate cultures. Environ Microbiol 3(6):380–396

    CAS  PubMed  Google Scholar 

  • Anderson DM (1998) Physiology and bloom dynamics of toxic Alexandrium species, with emphasis on life cycle transitions. Nato ASI Ser G Ecol Sci 41:29–48

    Google Scholar 

  • Andrews S (2010) FastQC: a quality control tool for high throughput sequence data. http://www.bioinformatics.babraham.ac.uk/projects/fastqc. Accesed May 2017

  • Appiah AA, Van WP, Osborne MC, Gow NA (2005) Potassium homeostasis influences the locomotion and encystment of zoospores of plant pathogenic oomycetes. Fungal Genet Biol 42(3):213–223

    CAS  PubMed  Google Scholar 

  • Bayer T, Aranda M, Sunagawa S, Yum LK, DeSalvo MK, Lindquist E, Coffroth MA, Voolstra CR, Medina M (2012) Symbiodinium transcriptomes: genome insights into the dinoflagellate symbionts of reef-building corals. PLoS One 7(4):e35269

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bogus K, Mertens KN, Lauwaert J, Harding IC, Vrielinck H, Zonneveld KA, Versteegh GJ (2014) Differences in the chemical composition of organic-walled dinoflagellate resting cysts from phototrophic and heterotrophic dinoflagellates. J Phycol 50(2):254–266

    CAS  PubMed  Google Scholar 

  • Bolch CJ, Subramanian TA, Green DH (2011) The toxic dinoflagellate Gymnodinium catenatum (Dinophyceae) requires marine bacteria for growth. J Phycol 47(5):1009–1022

    PubMed  Google Scholar 

  • Bolger AM, Lohse M, Usadel B (2014) Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30(15):2114–2120

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bravo I, Figueroa RI (2014) Towards an ecological understanding of dinoflagellate cyst functions. Microorganisms 2(1):11–32

    PubMed  PubMed Central  Google Scholar 

  • Buchfink B, Xie C, Huson DH (2015) Fast and sensitive protein alignment using DIAMOND. Nat Methods 12(1):59–60

    CAS  PubMed  Google Scholar 

  • Burton M, Rose TM, Færgeman NJ, Knudsen J (2005) Evolution of the acyl-CoA binding protein (ACBP). Biochem J 392(2):299–307

    CAS  PubMed  PubMed Central  Google Scholar 

  • Caron DA, Alexander H, Allen AE, Archibald JM et al (2017) Probing the evolution, ecology and physiology of marine protists using transcriptomics. Nat Rev Microbiol 15(1):6

    CAS  PubMed  Google Scholar 

  • Chambouvet A, Morin P, Marie D, Guillou L (2008) Control of toxic marine dinoflagellate blooms by serial parasitic killers. Science 322(5905):1254–1257

    CAS  PubMed  Google Scholar 

  • Chen S, McElroy JS, Dane F, Peatman E (2015) Optimizing transcriptome assemblies for Eleusine indica leaf and seedling by combining multiple assemblies from three de novo assemblers. Plant Genomics 8(1):1–10

    Google Scholar 

  • Cooper JT, Sinclair GA, Wawrik B (2016) Transcriptome analysis of Scrippsiella trochoidea CCMP 3099 reveals physiological changes related to nitrate depletion. Front Microbiol 7:639

    PubMed  PubMed Central  Google Scholar 

  • Croft MT, Lawrence AD, Raux-Deery E, Warren MJ, Smith AG (2005) Algae acquire vitamin B12 through a symbiotic relationship with bacteria. Nature 438(7064):90–93

    CAS  PubMed  Google Scholar 

  • Cruz-López R, Maske H (2016) The vitamin B1 and B12 required by the marine dinoflagellate Lingulodinium polyedrum can be provided by its associated bacterial community in culture. Front Microbiol 7:560

    PubMed  PubMed Central  Google Scholar 

  • Dale B, Yentsch CM, Hurst JW (1978) Toxicity in resting cysts of the red-tide dinoflagellate Gonyaulax excavata from deeper water coastal sediments. Science 201(4362):1223–1225

    CAS  PubMed  Google Scholar 

  • Deng Y, Hu Z, Shang L, Peng Q, Tang Y (2017) Transcriptomic analyses of Scrippsiella trochoidea revealed processes regulating encystment and dormancy in the life cycle of dinoflagellates, with a particular attention to the role of abscisic acid. Front Microbiol 8:2450

    PubMed  PubMed Central  Google Scholar 

  • Deutscher MP (2003) Degradation of stable RNA in bacteria. J Biol Chem 278(46):45041–45044

    CAS  PubMed  Google Scholar 

  • Du ZY, Chen MX, Chen QF, Xiao S, Chye ML (2013) Arabidopsis acyl-CoA-binding protein ACBP 1 participates in the regulation of seed germination and seedling development. Plant J 74(2):294–309

    CAS  PubMed  Google Scholar 

  • Ebenezer V, Ki JS (2012) Evaluation of the sub-lethal toxicity of Cu, Pb, bisphenol A and polychlorinated biphenyl to the marine dinoflagellate Cochlodinium polykrikoides. Algae 27(1):63

    CAS  Google Scholar 

  • Einarsson E, Troell K, Hoeppner MP, Grabherr M, Ribacke U, Svärd SG (2016) Coordinated changes in gene expression throughout encystation of Giardia intestinalis. PLoS Negl Trop Dis 10(3):e0004571

    PubMed  PubMed Central  Google Scholar 

  • Ellegaard M, Moestrup Ø (1999) Fine structure of the flagellar apparatus and morphological details of Gymnodinium nolleri sp. nov. (Dinophyceae), an unarmored dinoflagellate producing a microreticulate cyst. Phycologia 38(4):289–300

    Google Scholar 

  • Fenchel T (2001) How dinoflagellates swim. Protist 152(4):329–338

    CAS  PubMed  Google Scholar 

  • Furuichi T, Matsuura K (2016) Kinetic analysis on the motility of liverwort sperms using a microscopic computer-assisted sperm analyzing system. Environ Control Biol 54(1):45–49

    CAS  Google Scholar 

  • Gierz SL, Forêt S, Leggat W (2017) Transcriptomic analysis of thermally stressed Symbiodinium reveals differential expression of stress and metabolism genes. Front Plant Sci 8:271

    PubMed  PubMed Central  Google Scholar 

  • Gobler CJ, Berry DL, Anderson OR, Burson A et al (2008) Characterization, dynamics, and ecological impacts of harmful Cochlodinium polykrikoides blooms on eastern Long Island, NY, USA. Harmful Algae 7(3):293–307

    CAS  Google Scholar 

  • Goodstein DM, Shu S, Howson R, Neupane R et al (2011) Phytozome: a comparative platform for green plant genomics. Nucleic Acids Res 40(D1):D1178–D1186

    PubMed  PubMed Central  Google Scholar 

  • Grabherr MG, Haas BJ, Yassour M, Levin JZ et al (2011) Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat Biotechnol 29(7):644–652

    CAS  PubMed  PubMed Central  Google Scholar 

  • Guo R, Lim WA, Ki JS (2016a) Genome-wide analysis of transcription and photosynthesis inhibition in the harmful dinoflagellate Prorocentrum minimum in response to the biocide copper sulfate. Harmful Algae 57:27–38

    CAS  PubMed  Google Scholar 

  • Guo R, Wang H, Suh YS, Ki JS (2016b) Transcriptomic profiles reveal the genome-wide responses of the harmful dinoflagellate Cochlodinium polykrikoides when exposed to the algicide copper sulfate. BMC Genomics 17(1):29

    PubMed  PubMed Central  Google Scholar 

  • Harke MJ, Juhl AR, Haley ST, Alexander H, Dyhrman ST (2017) Conserved transcriptional responses to nutrient stress in bloom-forming algae. Front Microbiol 8:1279

    PubMed  PubMed Central  Google Scholar 

  • Hay RT (2005) SUMO: a history of modification. Mol Cell 18(1):1–12

    CAS  PubMed  Google Scholar 

  • Hou DY, Mao XT, Gu S, Li HY, Liu JS, Yang WD (2018) Systems-level analysis of metabolic mechanism following nitrogen limitation in benthic dinoflagellate Prorocentrum lima. Algal Res 33:389–398

    Google Scholar 

  • Huang DW, Sherman BT, Lempicki RA (2009) Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc 4(1):44–57

    CAS  Google Scholar 

  • Huelsenbeck JP, Ronquist F (2001) MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17(8):754–755

    CAS  PubMed  Google Scholar 

  • Inaba K (2003) Molecular architecture of the sperm flagella: molecules for motility and signaling. Zool Sci 20(9):1043–1056

    CAS  Google Scholar 

  • Isayenkov S, Isner JC, Maathuis FJ (2010) Vacuolar ion channels: roles in plant nutrition and signalling. FEBS Lett 584(10):1982–1988

    CAS  PubMed  Google Scholar 

  • Jang SH, Jeong HJ, Chon JK, Lee SY (2017a) De novo assembly and characterization of the transcriptome of the newly described dinoflagellate Ansanella granifera: spotlight on flagellum-associated genes. Mar Genomics 33:47–55

    PubMed  Google Scholar 

  • Jang SH, Jeong HJ, Moestrup Ø, Kang NS, Lee SY, Lee KH, Seong KA (2017b) Yihiella yeosuensis gen. et sp. nov. (Suessiaceae, Dinophyceae), a novel dinoflagellate isolated from the coastal waters of Korea. J Phycol 53(1):131–145

    CAS  PubMed  Google Scholar 

  • Jang SH, Jeong HJ, Kwon JE, Lee KH (2017c) Mixotrophy in the newly described dinoflagellate Yihiella yeosuensis: a small, fast dinoflagellate predator that grows mixotrophically, but not autotrophically. Harmful Algae 62:94–103

    PubMed  Google Scholar 

  • Jeong HJ, Yoo YD, Kim JS, Seong KA, Kang NS, Kim TH (2010) Growth, feeding and ecological roles of the mixotrophic and heterotrophic dinoflagellates in marine planktonic food webs. Ocean Sci J 45(2):65–69

    CAS  Google Scholar 

  • Jeong HJ, Lim AS, Franks PJ, Lee KH et al (2015) A hierarchy of conceptual models of red-tide generation: nutrition, behavior, and biological interactions. Harmful Algae 47:97–115

    Google Scholar 

  • Jeong HJ, Lim AS, Lee K, Lee MJ et al (2017) Ichthyotoxic Cochlodinium polykrikoides red tides offshore in the South Sea, Korea in 2014: I. Temporal variations in three-dimensional distributions of red-tide organisms and environmental factors. Algae 32(2):101–130

    CAS  Google Scholar 

  • Jeong HJ, Kang HC, You JH, Jang SH (2018) Interactions between the newly described small-and fast-swimming mixotrophic dinoflagellate Yihiella yeosuensis and common heterotrophic protists. J Eukaryot Microbiol 65(5):612–626

    PubMed  Google Scholar 

  • Kamykowski D (1981) Laboratory experiments on the diurnal vertical migration of marine dinoflagellates through temperature gradients. Mar Biol 62(1):57–64

    Google Scholar 

  • Keeling PJ, Burki F, Wilcox HM, Allam B et al (2014) The Marine Microbial Eukaryote Transcriptome Sequencing Project (MMETSP): illuminating the functional diversity of eukaryotic life in the oceans through transcriptome sequencing. PLoS Biol 12(6):e1001889

    PubMed  PubMed Central  Google Scholar 

  • Kellmann R, Stuken A, Orr RJ, Svendsen HM, Jakobsen KS (2010) Biosynthesis and molecular genetics of polyketides in marine dinoflagellates. Mar Drugs 8(4):1011–1048

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kersey PJ, Allen JE, Allot A, Barba M et al (2017) Ensembl Genomes 2018: an integrated omics infrastructure for non-vertebrate species. Nucleic Acids Res 46(D1):D802–D808

    PubMed Central  Google Scholar 

  • Kohli GS, Campbell K, John U, Smith KF, Fraga S, Rhodes LL, Murray SA (2017) Role of modular polyketide synthases in the production of polyether ladder compounds in ciguatoxin-producing Gambierdiscus polynesiensis and G. excentricus (Dinophyceae). J Eukaryot Microbiol 64(5):691–706

    CAS  PubMed  Google Scholar 

  • Koshimizu S, Kofuji R, Sasaki-Sekimoto Y, Kikkawa M et al (2018) Physcomitrella MADS-box genes regulate water supply and sperm movement for fertilization. Nat Plants 4(1):36

    CAS  PubMed  Google Scholar 

  • Kozminaski KG, Johnson KA, Forscher P, Rosenbaum JL (1993) A motility in the eukaryotic flagellum unrelated to flagellar beating. Proc Natl Acad Sci USA 90(12):5519–5523

    Google Scholar 

  • Kremp A, Heiskanen AS (1999) Sexuality and cyst formation of the spring-bloom dinoflagellate Scrippsiella hangoei in the coastal northern Baltic Sea. Mar Biol 134(4):771–777

    Google Scholar 

  • Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33(7):1870–1874

    CAS  PubMed  PubMed Central  Google Scholar 

  • Landsberg JH (2002) The effects of harmful algal blooms on aquatic organisms. Rev Fish Sci 10(2):113–390

    Google Scholar 

  • Lauritano C, Luca DD, Ferrarini A, Avanzato C, Minio A, Esposito F, Ianora A (2017) De novo transcriptome of the cosmopolitan dinoflagellate Amphidinium carterae to identify enzymes with biotechnological potential. Sci Rep 7(1):11701

    PubMed  PubMed Central  Google Scholar 

  • Le Bescot N, Mahe F, Audic S, Dimier C, Garet MJ, Poulain J, Wincker P, Vargas CD, Siano R (2016) Global patterns of pelagic dinoflagellate diversity across protist size classes unveiled by metabarcoding. Environ Microbiol 18(2):609–626

    PubMed  Google Scholar 

  • Leadbeater BT, Dodge JD (1967) An electron microscope study of dinoflagellate flagella. Microbiology 46(2):305–314

    CAS  Google Scholar 

  • Lee SK, Jeong HJ, Jang SH, Lee KH, Kang NS, Lee MJ, Potvin É (2014) Mixotrophy in the newly described dinoflagellate Ansanella granifera: feeding mechanism, prey species, and effect of prey concentration. Algae 29(2):137–152

    Google Scholar 

  • Li B, Dewey CN (2011) RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinform 12(1):323

    CAS  Google Scholar 

  • Li W, Godzik A (2006) Cd-hit: a fast program for clustering and comparing large sets of protein or nucleotide sequences. Bioinformatics 22(13):1658–1659

    CAS  PubMed  Google Scholar 

  • Lin S (2011) Genomic understanding of dinoflagellates. Res Microbiol 162(6):551–569

    CAS  PubMed  Google Scholar 

  • Lirdwitayaprasit T, Okaichi T, Montani S, Ochi T, Anderson DM (1990) Changes in cell chemical composition during the life cycle of Scrippsiella trochoidea (Dinophyceae). J Phycol 26(2):299–306

    CAS  Google Scholar 

  • Lowe CD, Mello LV, Samatar N, Martin LE, Montagnes DJ, Watts PC (2011) The transcriptome of the novel dinoflagellate Oxyrrhis marina (Alveolata: Dinophyceae): response to salinity examined by 454 sequencing. BMC Genomics 12(1):519

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lu Y, Wohlrab S, Groth M, Glöckner G, Guillou L, John U (2016) Transcriptomic profiling of Alexandrium fundyense during physical interaction with or exposure to chemical signals from the parasite Amoebophrya. Mol Ecol 25(6):1294–1307

    CAS  PubMed  Google Scholar 

  • Marchler-Bauer A, Bo Y, Han L, He J et al (2017) CDD/SPARCLE: functional classification of proteins via subfamily domain architectures. Nucleic Acids Res 45:D200–D203

    CAS  PubMed  Google Scholar 

  • Mendez GS, Delwiche CF, Apt KE, Lippmeier JC (2015) Dinoflagellate gene structure and intron splice sites in a genomic tandem array. J Eukaryot Microbiol 62(5):679–687

    CAS  PubMed  PubMed Central  Google Scholar 

  • Montresor M, Nuzzo L, Mazzocchi MG (2003) Viability of dinoflagellate cysts after the passage through the copepod gut. J Exp Mar Biol Ecol 287(2):209–221

    Google Scholar 

  • Murray SA, Suggett DJ, Doblin MA, Kohli GS, Seymour JR, Fabris M, Ralph PJ (2016) Unravelling the functional genetics of dinoflagellates: a review of approaches and opportunities. Perspect Phycol 3(1):37–52

    Google Scholar 

  • Oda T, Yanagisawa H, Yagi T, Kikkawa M (2014) Mechanosignaling between central apparatus and radial spokes controls axonemal dynein activity. J Cell Biol 204(5):807–819

    CAS  PubMed  PubMed Central  Google Scholar 

  • Park TG, Lim WA, Park YT, Lee CK, Jeong HJ (2013) Economic impact, management and mitigation of red tides in Korea. Harmful Algae 30:S131–S143

    Google Scholar 

  • Pazour GJ, Agrin N, Leszyk J, Witman GB (2005) Proteomic analysis of a eukaryotic cilium. J Cell Biol 170(1):103–113

    CAS  PubMed  PubMed Central  Google Scholar 

  • Poulsen NC, Spector I, Spurck TP, Schultz TF, Wetherbee R (1999) Diatom gliding is the result of an actin-myosin motility system. Cell Motil Cytoskelet 44(1):23–33

    CAS  Google Scholar 

  • R Core Team (2017) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

    Google Scholar 

  • Ridge RW, Hori T, Miyamura SI (1997) Analysis of flagellar movement in Ginkgo biloba sperm by high speed video microscopy. Ginkgo biloba a global treasure. Springer, Tokyo, pp 99–107

    Google Scholar 

  • Rokitta SD, de Nooijer LJ, Trimborn S, de Vargas C, Rost B, John U (2011) Transcriptome analyses reveal differential gene expression patterns between the life-cycle stages of Emiliania huxleyi (Haptophyta) and reflect specialization to different ecological niches. J Phycol 47:829–838

    CAS  PubMed  Google Scholar 

  • Rosenbaum J (2000) Cytoskeleton: functions for tubulin modifications at last. Curr Biol 10(21):R801–R803

    CAS  PubMed  Google Scholar 

  • Rosenbaum JL, Witman GB (2002) Intraflagellar transport. Nat Rev Mol Cell Biol 3(11):813

    CAS  PubMed  Google Scholar 

  • Roy S, Letourneau L, Morse D (2014) Cold-induced cysts of the photosynthetic dinoflagellate Lingulodinium polyedrum have an arrested circadian bioluminescence rhythm and lower levels of protein phosphorylation. Plant Physiol 164(2):966–977

    CAS  PubMed  Google Scholar 

  • Ryan DE, Campbell L (2016) Identification and phylogeny of putative PEPC genes in three toxin-producing Karenia (Dinophyta) species. J Phycol 52(4):618–625

    CAS  PubMed  Google Scholar 

  • Selvin RC, Lewis CM, Yentsch CM, Hurst JW (1984) Seasonal persistence of resting cyst toxicity in the dinoflagellate Gonyaulax tamarensis var. excavata. Toxicon 22(5):817–820

    CAS  PubMed  Google Scholar 

  • Shen B (2003) Polyketide biosynthesis beyond the type I, II and III polyketide synthase paradigms. Curr Opin Chem Biol 7(2):285–295

    CAS  PubMed  Google Scholar 

  • Sheng J, Malkiel E, Katz J, Adolf J, Belas R, Place AR (2007) Digital holographic microscopy reveals prey-induced changes in swimming behavior of predatory dinoflagellates. Proc Natl Acad Sci USA 104(44):17512–17517

    CAS  PubMed  PubMed Central  Google Scholar 

  • Shi X, Lin X, Li L, Li M, Palenik B, Lin S (2017) Transcriptomic and microRNAomic profiling reveals multi-faceted mechanisms to cope with phosphate stress in a dinoflagellate. ISME J 11(10):2209

    CAS  PubMed  PubMed Central  Google Scholar 

  • Stoecker DK, Hansen PJ, Caron DA, Mitra A (2017) Mixotrophy in the marine plankton. Annu Rev Mar Sci 9:311–335

    Google Scholar 

  • Taylor FJR, Hoppenrath M, Saldarriaga JF (2008) Dinoflagellate diversity and distribution. Biodivers Conserv 17(2):407–418

    Google Scholar 

  • Testo WL, Watkins JE, Barrington DS (2015) Dynamics of asymmetrical hybridization in North American wood ferns: reconciling patterns of inheritance with gametophyte reproductive biology. New Phytol 206(2):785–795

    CAS  PubMed  Google Scholar 

  • Van Dolah FM, Kohli GS, Morey JS, Murray SA (2017) Both modular and single-domain Type I polyketide synthases are expressed in the brevetoxin-producing dinoflagellate, Karenia brevis (Dinophyceae). J Phycol 53(6):1325–1339

    PubMed  PubMed Central  Google Scholar 

  • Vijay N, Poelstra JW, Künstner A, Wolf JB (2013) Challenges and strategies in transcriptome assembly and differential gene expression quantification. A comprehensive in silico assessment of RNA-seq experiments. Mol Ecol 22(3):620–634

    CAS  PubMed  Google Scholar 

  • Von Dassow P, Ogata H, Probert I, Wincker P, Da Silva C, Audic S, Claverie JM, de Vargas C (2009) Transcriptome analysis of functional differentiation between haploid and diploid cells of Emiliania huxleyi, a globally significant photosynthetic calcifying cell. Genome Biol 10(10):R114

    Google Scholar 

  • Ward W, Alvarado L, Rawlings ND, Engel JC, Franklin C, McKerrow JH (1997) A primitive enzyme for a primitive cell: the protease required for excystation of Giardia. Cell 89(3):437–444

    CAS  PubMed  Google Scholar 

  • Webster DR, Cooksey KE, Rubin RW (1985) An investigation of the involvement of cytoskeletal structures and secretion in gliding motility of the marine diatom, Amphora coffeaeformis. Cell Motil 5(2):103–122

    CAS  Google Scholar 

  • Wei Q, Zhang Y, Li Y, Zhang Q, Ling K, Hu J (2012) The BBSome controls IFT assembly and turnaround in cilia. Nat Cell Biol 14(9):950

    PubMed  PubMed Central  Google Scholar 

  • Wiebe HH (1978) The significance of plant vacuoles. Bioscience 28(5):327–331

    Google Scholar 

  • Wolf JB (2013) Principles of transcriptome analysis and gene expression quantification: an RNA-seq tutorial. Mol Ecol Resour 13(4):559–572

    CAS  PubMed  Google Scholar 

  • Xiang T, Nelson W, Rodriguez J, Tolleter D, Grossman AR (2015) Symbiodinium transcriptome and global responses of cells to immediate changes in light intensity when grown under autotrophic or mixotrophic conditions. Plant J 82(1):67–80

    CAS  PubMed  Google Scholar 

  • Yang Y, Smith SA (2013) Optimizing de novo assembly of short-read RNA-seq data for phylogenomics. BMC Genomics 14(1):328

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ye J, Fang L, Zheng H, Zhang Y et al (2006) WEGO: a web tool for plotting GO annotations. Nucleic Acids Res 34(suppl 2):W293–W297

    CAS  PubMed  PubMed Central  Google Scholar 

  • Yu L, Lin S, Zhang H (2018) Transcriptomic responses to thermal stress and varied phosphorus conditions in Symbiodinium kawagutii. bioRxiv 499210

  • Zeng B, Cai X, Zhu G (2006) Functional characterization of a fatty acyl-CoA-binding protein (ACBP) from the apicomplexan Cryptosporidium parvum. Microbiology 152(8):2355–2363

    CAS  PubMed  Google Scholar 

  • Zhu G, LaGier MJ, Stejskal F, Millership JJ, Cai X, Keithly JS (2002) Cryptosporidium parvum: the first protist known to encode a putative polyketide synthase. Gene 298:79–89

    CAS  PubMed  Google Scholar 

  • Zonneveld KA, Versteegh G, Kodrans-Nsiah M (2008) Preservation and organic chemistry of Late Cenozoic organic-walled dinoflagellate cysts: a review. Mar Micropaleontol 68(1–2):179–197

    Google Scholar 

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Acknowledgements

This research was supported by the useful dinoflagellate program of Korea Institute of Marine Science and Technology Promotion (KIMST) funded by the Ministry of Oceans and Fisheries (MOF) and the National Research Foundation (NRF) funded by the Ministry of Science and ICT (NRF-2015M1A5A1041806 and NRF-2017R1E1A1A01074419) award to HJJ.

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  1. School of Earth and Environmental Sciences, College of Natural Sciences, Seoul National University, Seoul, 08826, Republic of Korea

    Se Hyeon Jang & Hae Jin Jeong

  2. Advanced Institutes of Convergence Technology, Suwon, Gyeonggi-do, 16229, Republic of Korea

    Hae Jin Jeong

  3. Macrogen Inc., Seoul, 08511, Republic of Korea

    Jae Kyung Chon

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Jang, S.H., Jeong, H.J. & Chon, J.K. De novo transcriptome of the newly described phototrophic dinoflagellate Yihiella yeosuensis: comparison between vegetative cells and cysts. Mar Biol 166, 104 (2019). https://doi.org/10.1007/s00227-019-3554-9

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