Draft assembly of the symbiodinium minutum nuclear genome reveals dinoflagellate gene structure

Eiichi Shoguchi, Chuya Shinzato, Takeshi Kawashima, Fuki Gyoja, Sutada Mungpakdee, Ryo Koyanagi, Takeshi Takeuchi, Kanako Hisata, Makiko Tanaka, Mayuki Fujiwara, Mayuko Hamada, Azadeh Seidi, Manabu Fujie, Takeshi Usami, Hiroki Goto, Shinichi Yamasaki, Nana Arakaki, Yutaka Suzuki, Sumio Sugano, Atsushi Toyoda & 6 others Yoko Kuroki, Asao Fujiyama, Mónica Medina, Mary Alice Coffroth, Debashish Bhattacharya, Nori Satoh

    Research output: Contribution to journalArticle

    208 Citations (Scopus)

    Abstract

    Background Dinoflagellates are known for their capacity to form harmful blooms (e.g., "red tides") and as symbiotic, photosynthetic partners for corals. These unicellular eukaryotes have permanently condensed, liquid-crystalline chromosomes and immense nuclear genome sizes, often several times the size of the human genome. Here we describe the first draft assembly of a dinoflagellate nuclear genome, providing insights into its genome organization and gene inventory. Results Sequencing reads from Symbiodinium minutum were assembled into 616 Mbp gene-rich DNA regions that represented roughly half of the estimated 1,500 Mbp genome of this species. The assembly encoded ∼42,000 protein-coding genes, consistent with previous dinoflagellate gene number estimates using transcriptomic data. The Symbiodinium genome contains duplicated genes for regulator of chromosome condensation proteins, nearly one-third of which have eukaryotic orthologs, whereas the remainder have most likely been acquired through bacterial horizontal gene transfers. Symbiodinium genes are enriched in spliceosomal introns (mean = 18.6 introns/gene). Donor and acceptor splice sites are unique, with 5′ sites utilizing not only GT but also GC and GA, whereas at 3′ sites, a conserved G is present after AG. All spliceosomal snRNA genes (U1-U6) are clustered in the genome. Surprisingly, the Symbiodinium genome displays unidirectionally aligned genes throughout the genome, forming a cluster-like gene arrangement. Conclusions We show here that a dinoflagellate genome exhibits unique and divergent characteristics when compared to those of other eukaryotes. Our data elucidate the organization and gene inventory of dinoflagellates and lay the foundation for future studies of this remarkable group of eukaryotes.

    Original languageEnglish
    Pages (from-to)1399-1408
    Number of pages10
    JournalCurrent Biology
    Volume23
    Issue number15
    DOIs
    Publication statusPublished - Aug 5 2013

    Fingerprint

    Dinoflagellida
    Symbiodinium
    nuclear genome
    Genes
    Genome
    genome
    genes
    Eukaryota
    RNA Splice Sites
    eukaryotic cells
    Introns
    Chromosomes
    Harmful Algal Bloom
    introns
    Bacterial Genes
    Genome Size
    Horizontal Gene Transfer
    Equipment and Supplies
    Anthozoa
    Gene Order

    All Science Journal Classification (ASJC) codes

    • Biochemistry, Genetics and Molecular Biology(all)
    • Agricultural and Biological Sciences(all)

    Cite this

    Shoguchi, E., Shinzato, C., Kawashima, T., Gyoja, F., Mungpakdee, S., Koyanagi, R., ... Satoh, N. (2013). Draft assembly of the symbiodinium minutum nuclear genome reveals dinoflagellate gene structure. Current Biology, 23(15), 1399-1408. https://doi.org/10.1016/j.cub.2013.05.062

    Draft assembly of the symbiodinium minutum nuclear genome reveals dinoflagellate gene structure. / Shoguchi, Eiichi; Shinzato, Chuya; Kawashima, Takeshi; Gyoja, Fuki; Mungpakdee, Sutada; Koyanagi, Ryo; Takeuchi, Takeshi; Hisata, Kanako; Tanaka, Makiko; Fujiwara, Mayuki; Hamada, Mayuko; Seidi, Azadeh; Fujie, Manabu; Usami, Takeshi; Goto, Hiroki; Yamasaki, Shinichi; Arakaki, Nana; Suzuki, Yutaka; Sugano, Sumio; Toyoda, Atsushi; Kuroki, Yoko; Fujiyama, Asao; Medina, Mónica; Coffroth, Mary Alice; Bhattacharya, Debashish; Satoh, Nori.

    In: Current Biology, Vol. 23, No. 15, 05.08.2013, p. 1399-1408.

    Research output: Contribution to journalArticle

    Shoguchi, E, Shinzato, C, Kawashima, T, Gyoja, F, Mungpakdee, S, Koyanagi, R, Takeuchi, T, Hisata, K, Tanaka, M, Fujiwara, M, Hamada, M, Seidi, A, Fujie, M, Usami, T, Goto, H, Yamasaki, S, Arakaki, N, Suzuki, Y, Sugano, S, Toyoda, A, Kuroki, Y, Fujiyama, A, Medina, M, Coffroth, MA, Bhattacharya, D & Satoh, N 2013, 'Draft assembly of the symbiodinium minutum nuclear genome reveals dinoflagellate gene structure', Current Biology, vol. 23, no. 15, pp. 1399-1408. https://doi.org/10.1016/j.cub.2013.05.062
    Shoguchi E, Shinzato C, Kawashima T, Gyoja F, Mungpakdee S, Koyanagi R et al. Draft assembly of the symbiodinium minutum nuclear genome reveals dinoflagellate gene structure. Current Biology. 2013 Aug 5;23(15):1399-1408. https://doi.org/10.1016/j.cub.2013.05.062
    Shoguchi, Eiichi ; Shinzato, Chuya ; Kawashima, Takeshi ; Gyoja, Fuki ; Mungpakdee, Sutada ; Koyanagi, Ryo ; Takeuchi, Takeshi ; Hisata, Kanako ; Tanaka, Makiko ; Fujiwara, Mayuki ; Hamada, Mayuko ; Seidi, Azadeh ; Fujie, Manabu ; Usami, Takeshi ; Goto, Hiroki ; Yamasaki, Shinichi ; Arakaki, Nana ; Suzuki, Yutaka ; Sugano, Sumio ; Toyoda, Atsushi ; Kuroki, Yoko ; Fujiyama, Asao ; Medina, Mónica ; Coffroth, Mary Alice ; Bhattacharya, Debashish ; Satoh, Nori. / Draft assembly of the symbiodinium minutum nuclear genome reveals dinoflagellate gene structure. In: Current Biology. 2013 ; Vol. 23, No. 15. pp. 1399-1408.
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    title = "Draft assembly of the symbiodinium minutum nuclear genome reveals dinoflagellate gene structure",
    abstract = "Background Dinoflagellates are known for their capacity to form harmful blooms (e.g., {"}red tides{"}) and as symbiotic, photosynthetic partners for corals. These unicellular eukaryotes have permanently condensed, liquid-crystalline chromosomes and immense nuclear genome sizes, often several times the size of the human genome. Here we describe the first draft assembly of a dinoflagellate nuclear genome, providing insights into its genome organization and gene inventory. Results Sequencing reads from Symbiodinium minutum were assembled into 616 Mbp gene-rich DNA regions that represented roughly half of the estimated 1,500 Mbp genome of this species. The assembly encoded ∼42,000 protein-coding genes, consistent with previous dinoflagellate gene number estimates using transcriptomic data. The Symbiodinium genome contains duplicated genes for regulator of chromosome condensation proteins, nearly one-third of which have eukaryotic orthologs, whereas the remainder have most likely been acquired through bacterial horizontal gene transfers. Symbiodinium genes are enriched in spliceosomal introns (mean = 18.6 introns/gene). Donor and acceptor splice sites are unique, with 5′ sites utilizing not only GT but also GC and GA, whereas at 3′ sites, a conserved G is present after AG. All spliceosomal snRNA genes (U1-U6) are clustered in the genome. Surprisingly, the Symbiodinium genome displays unidirectionally aligned genes throughout the genome, forming a cluster-like gene arrangement. Conclusions We show here that a dinoflagellate genome exhibits unique and divergent characteristics when compared to those of other eukaryotes. Our data elucidate the organization and gene inventory of dinoflagellates and lay the foundation for future studies of this remarkable group of eukaryotes.",
    author = "Eiichi Shoguchi and Chuya Shinzato and Takeshi Kawashima and Fuki Gyoja and Sutada Mungpakdee and Ryo Koyanagi and Takeshi Takeuchi and Kanako Hisata and Makiko Tanaka and Mayuki Fujiwara and Mayuko Hamada and Azadeh Seidi and Manabu Fujie and Takeshi Usami and Hiroki Goto and Shinichi Yamasaki and Nana Arakaki and Yutaka Suzuki and Sumio Sugano and Atsushi Toyoda and Yoko Kuroki and Asao Fujiyama and M{\'o}nica Medina and Coffroth, {Mary Alice} and Debashish Bhattacharya and Nori Satoh",
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    AU - Shoguchi, Eiichi

    AU - Shinzato, Chuya

    AU - Kawashima, Takeshi

    AU - Gyoja, Fuki

    AU - Mungpakdee, Sutada

    AU - Koyanagi, Ryo

    AU - Takeuchi, Takeshi

    AU - Hisata, Kanako

    AU - Tanaka, Makiko

    AU - Fujiwara, Mayuki

    AU - Hamada, Mayuko

    AU - Seidi, Azadeh

    AU - Fujie, Manabu

    AU - Usami, Takeshi

    AU - Goto, Hiroki

    AU - Yamasaki, Shinichi

    AU - Arakaki, Nana

    AU - Suzuki, Yutaka

    AU - Sugano, Sumio

    AU - Toyoda, Atsushi

    AU - Kuroki, Yoko

    AU - Fujiyama, Asao

    AU - Medina, Mónica

    AU - Coffroth, Mary Alice

    AU - Bhattacharya, Debashish

    AU - Satoh, Nori

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    N2 - Background Dinoflagellates are known for their capacity to form harmful blooms (e.g., "red tides") and as symbiotic, photosynthetic partners for corals. These unicellular eukaryotes have permanently condensed, liquid-crystalline chromosomes and immense nuclear genome sizes, often several times the size of the human genome. Here we describe the first draft assembly of a dinoflagellate nuclear genome, providing insights into its genome organization and gene inventory. Results Sequencing reads from Symbiodinium minutum were assembled into 616 Mbp gene-rich DNA regions that represented roughly half of the estimated 1,500 Mbp genome of this species. The assembly encoded ∼42,000 protein-coding genes, consistent with previous dinoflagellate gene number estimates using transcriptomic data. The Symbiodinium genome contains duplicated genes for regulator of chromosome condensation proteins, nearly one-third of which have eukaryotic orthologs, whereas the remainder have most likely been acquired through bacterial horizontal gene transfers. Symbiodinium genes are enriched in spliceosomal introns (mean = 18.6 introns/gene). Donor and acceptor splice sites are unique, with 5′ sites utilizing not only GT but also GC and GA, whereas at 3′ sites, a conserved G is present after AG. All spliceosomal snRNA genes (U1-U6) are clustered in the genome. Surprisingly, the Symbiodinium genome displays unidirectionally aligned genes throughout the genome, forming a cluster-like gene arrangement. Conclusions We show here that a dinoflagellate genome exhibits unique and divergent characteristics when compared to those of other eukaryotes. Our data elucidate the organization and gene inventory of dinoflagellates and lay the foundation for future studies of this remarkable group of eukaryotes.

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