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 ToyodaYoko Kuroki, Asao Fujiyama, Mónica Medina, Mary Alice Coffroth, Debashish Bhattacharya, Nori Satoh

Research output: Contribution to journalArticle

224 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
Externally publishedYes

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

ASJC Scopus subject areas

  • Agricultural and Biological Sciences(all)
  • Biochemistry, Genetics and Molecular Biology(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.
@article{a97f26523ef040a0b7849ce85ade62aa,
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",
year = "2013",
month = "8",
day = "5",
doi = "10.1016/j.cub.2013.05.062",
language = "English",
volume = "23",
pages = "1399--1408",
journal = "Current Biology",
issn = "0960-9822",
publisher = "Cell Press",
number = "15",

}

TY - JOUR

T1 - Draft assembly of the symbiodinium minutum nuclear genome reveals dinoflagellate gene structure

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

PY - 2013/8/5

Y1 - 2013/8/5

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.

AB - 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.

UR - http://www.scopus.com/inward/record.url?scp=84881317368&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=84881317368&partnerID=8YFLogxK

U2 - 10.1016/j.cub.2013.05.062

DO - 10.1016/j.cub.2013.05.062

M3 - Article

C2 - 23850284

AN - SCOPUS:84881317368

VL - 23

SP - 1399

EP - 1408

JO - Current Biology

JF - Current Biology

SN - 0960-9822

IS - 15

ER -