The 100%-Complete Nuclear and Organellar Genome Sequences of the Ultrasmall Red Algal Species Cyanidioschyzon merolae 10D

  • Hisayoshi NozakiEmail author
  • Yu Kanesaki
  • Motomichi Matsuzaki
  • Shunsuke Hirooka


We were the first group to successfully sequence the 100%-complete entire eukaryotic genome in 2007, mainly using automated Sanger sequencing of the unicellular, ultrasmall red algal species Cyanidioschyzon merolae 10D. This world record was principally based on the ultrasmall size of the C. merolae genome (ca. 16 megabase pairs) as well as on three excellent previous studies: the 100%-complete mitochondrial genome in 1998, the 100%-complete plastid genome in 2003, and the first algal cell nuclear genome in 2004. The 100%-complete nuclear sequences demonstrated that this ultrasmall red alga contains unusually simple sets of genes and genetic sequences. For example, because introns are lacking in almost all of the protein-coding nuclear genes of C. merolae, the 100%-complete sequence can be used to directly deduce the sequences of all C. merolae proteins, which will be extremely valuable in further proteomics research. Thus, this small red alga represents an ideal model organism for studying the fundamental relationships among the plastid, mitochondrial, and nuclear genomes. The 100%-complete nuclear genome sequence has greatly improved the precision and value of biological analyses of C. merolae.


Algal genome Cyanidioschyzon merolae Eukaryotic cell Mitochondrial genome Nuclear genome 100%-complete genome Plastid genome Red alga 



HN was supported by a Grant-in-Aid for Scientific Research (grant number 16H02518) from the Ministry of Education, Culture, Sports, Science and Technology (MEXT)/Japan Society for the Promotion of Science (JSPS) KAKENHI.


  1. Barbier G, Oesterhelt C et al (2005) Comparative genomics of two closely related unicellular thermo-acidophilic red algae, Galdieria sulphuraria and Cyanidioschyzon merolae, reveals the molecular basis of the metabolic flexibility of Galdieria sulphuraria and significant differences in carbohydrate metabolism of both algae. Plant Physiol, 137:460–474.
  2. Cleveland DW, Mao Y et al (2003) Centromeres and kinetochores: from epigenetics to mitotic checkpoint signaling. Cell 112:407–421. CrossRefPubMedGoogle Scholar
  3. Cunningham FX Jr, Lee H et al (2006) Carotenoid biosynthesis in the primitive red alga Cyanidioschyzon merolae. Eukaryot Cell 6:533–545. CrossRefPubMedPubMedCentralGoogle Scholar
  4. Curtis BA, Tanifuji G et al (2012) Algal genomes reveal evolutionary mosaicism and the fate of nucleomorphs. Nature 492:59–65. CrossRefPubMedGoogle Scholar
  5. Derelle E, Ferraz C et al (2006) Genome analysis of the smallest free-living eukaryote Ostreococcus tauri unveils many unique features. Proc Natl Acad Sci U S A 103:11647–11652. CrossRefPubMedPubMedCentralGoogle Scholar
  6. Fujiwara T, Misumi O et al (2009) Periodic gene expression patterns during the highly synchronized cell nucleus and organelle division cycles in the unicellular red alga Cyanidioschyzon merolae. DNA Res 16:59–72. CrossRefPubMedPubMedCentralGoogle Scholar
  7. Fujiwara T, Ohnuma M et al (2013a) Gene targeting in the red alga Cyanidioschyzon merolae: single- and multi-copy insertion using authentic and chimeric selection markers. PLoS One 8:e73608. CrossRefPubMedPubMedCentralGoogle Scholar
  8. Fujiwara T, Tanaka K et al (2013b) Spatiotemporal dynamics of condensins I and II: evolutionary insights from the primitive red alga Cyanidioschyzon merolae. Mol Biol Cell 24:2515–2527. CrossRefPubMedPubMedCentralGoogle Scholar
  9. Fujiwara T, Kanesaki Y et al (2015) A nitrogen source-dependent inducible and repressible gene expression system in the red alga Cyanidioschyzon merolae. Front Plant Sci 6:657. PubMedPubMedCentralGoogle Scholar
  10. Hanschen ER, Marriage TN et al (2016) The Gonium pectorale genome demonstrates co-option of cell cycle regulation during the evolution of multicellularity. Nat Commun 7:11370. CrossRefPubMedPubMedCentralGoogle Scholar
  11. Imamura S, Kanesaki Y et al (2009) R2R3-type MYB transcription factor, CmMYB1, is a central nitrogen assimilation regulator in Cyanidioschyzon merolae. Proc Natl Acad Sci U S A 106:12548–12553. CrossRefPubMedPubMedCentralGoogle Scholar
  12. Imoto Y, Kuroiwa H et al (2013) Single-membrane-bounded peroxisome division revealed by isolation of dynamin-based machinery. Proc Natl Acad Sci U S A 110:9583–9588. CrossRefPubMedPubMedCentralGoogle Scholar
  13. Janouškovec J, Liu S-L et al (2013) Evolution of red algal plastid genomes: ancient architectures, introns, horizontal gene transfer, and taxonomic utility of plastid markers. PLoS One 8:e59001. CrossRefPubMedPubMedCentralGoogle Scholar
  14. Kaneko T, Sato S et al (1996) Sequence analysis of the genome of the unicellular cyanobacterium Synechocystis sp. strain PCC6803. II. Sequence determination of the entire genome and assignment of potential protein-coding regions. DNA Res 3:109–136CrossRefPubMedGoogle Scholar
  15. Kanesaki Y, Kobayashi Y et al (2009) Mg-protoporphyrin IX signaling in Cyanidioschyzon merolae: multiple pathways may involve the retrograde signaling in plant cells. Plant Signal Behav 4:1190–1192. CrossRefPubMedPubMedCentralGoogle Scholar
  16. Kanesaki Y, Imamura S et al (2012) External light conditions and internal cell cycle phases coordinate accumulation of chloroplast and mitochondrial transcripts in the red alga Cyanidioschyzon merolae. DNA Res 19:289–303. CrossRefPubMedPubMedCentralGoogle Scholar
  17. Kanesaki Y, Imamura S et al (2015) Identification of centromere regions in chromosomes of a unicellular red alga, Cyanidioschyzon merolae. FEBS Lett 589:1219–1224. CrossRefPubMedGoogle Scholar
  18. Kuroiwa T (1982) Mitochondrial nuclei. Int Rev Cytol 75:1–59CrossRefPubMedGoogle Scholar
  19. Martin W, Rujan T et al (2002) Evolutionary analysis of Arabidopsis, cyanobacterial, and chloroplast genomes reveals plastid phylogeny and thousands of cyanobacterial genes in the nucleus. Proc Natl Acad Sci U S A 99:12246–11251. CrossRefPubMedPubMedCentralGoogle Scholar
  20. Maruyama S, Kuroiwa H et al (2007) Centromere dynamics in the primitive red alga Cyanidioschyzon merolae. Plant J 49:1122–1129. CrossRefPubMedGoogle Scholar
  21. Maruyama S, Matsuzaki M et al (2008) Centromere structures highlighted by the 100%-complete Cyanidioschyzon merolae genome. Plant Signal Behav 3:140–141. CrossRefPubMedPubMedCentralGoogle Scholar
  22. Matsuzaki M, Misumi O et al (2004) Genome sequence of the ultrasmall unicellular red alga Cyanidioschyzon merolae 10D. Nature 428:653–657. CrossRefPubMedGoogle Scholar
  23. Minoda A, Sakagami R et al (2004) Improvement of culture conditions and evidence for nuclear transformation by homologous recombination in a red alga, Cyanidioschyzon merolae 10D. Plant Cell Physiol 45:667–671. CrossRefPubMedGoogle Scholar
  24. Minoda A, Nagasawa K et al (2005) Microarray profiling of plastid gene expression in a unicellular red alga, Cyanidioschyzon merolae. Plant Mol Biol 59:375–385. CrossRefPubMedGoogle Scholar
  25. Misumi O, Matsuzaki M et al (2005) Cyanidioschyzon merolae genome. A tool for facilitating comparable studies on organelle biogenesis in photosynthetic eukaryotes. Plant Physiol 137:567–585. CrossRefPubMedPubMedCentralGoogle Scholar
  26. Nozaki H, Ohta N et al (2003) Phylogeny of plastids based on cladistic analysis of gene loss inferred from complete plastid genome sequences. J Mol Evol 57:377–382. CrossRefPubMedGoogle Scholar
  27. Nozaki H, Takano H et al (2007) A 100%-complete sequence reveals unusually simple genomic features in the hot-spring red alga Cyanidioschyzon merolae. BMC Biol 5:28. CrossRefPubMedPubMedCentralGoogle Scholar
  28. Ohta N, Sato N et al (1998) Structure and organization of the mitochondrial genome of the unicellular red alga Cyanidioschyzon merolae deduced from the complete nucleotide sequence. Nucleic Acids Res 26:5190–5198CrossRefPubMedPubMedCentralGoogle Scholar
  29. Ohta N, Matsuzaki M et al (2003) Complete sequence and analysis of the plastid genome of the unicellular red alga Cyanidioschyzon merolae. DNA Res 10:67–77CrossRefPubMedGoogle Scholar
  30. Ohyama K, Fukuzawa H et al (1986) Chloroplast gene organization deduced from complete sequence of liverwort Marchantia polymorpha chloroplast DNA. Nature 322:572–574CrossRefGoogle Scholar
  31. Schönknecht G, Chen WH et al (2013) Gene transfer from bacteria and archaea facilitated evolution of an extremophilic eukaryote. Science 339:1207–1210. CrossRefPubMedGoogle Scholar
  32. Session AM, Uno Y et al (2016) Genome evolution in the allotetraploid frog Xenopus laevis. Nature 538:336–343. CrossRefPubMedPubMedCentralGoogle Scholar
  33. Shinozaki K, Ohme M et al (1986) The complete nucleotide sequence of the tobacco chloroplast genome: its gene organization and expression. EMBO J 5:2043–2049PubMedPubMedCentralGoogle Scholar
  34. Sumiya N, Fujiwara T et al (2014) Development of a heat-shock inducible gene expression system in the red alga Cyanidioschyzon merolae. PLoS One 9:e111261. CrossRefPubMedPubMedCentralGoogle Scholar
  35. Tajima N, Sato S et al (2014) Analysis of the complete plastid genome of the unicellular red alga Porphyridium purpureum. J Plant Res 127:389–397. CrossRefPubMedGoogle Scholar
  36. Taki K, Sone T, Kobayashi Y, Watanabe S, Imamura S, Tanaka K (2015) Construction of a URA5.3 deletion strain of the unicellular red alga Cyanidioschyzon merolae: a background less host strain for transformation experiments. J Gen Appl Microbiol 61:211–214.
  37. Yang EC, Kim KM et al (2015) Highly conserved mitochondrial genomes among multicellular red algae of the Florideophyceae. Genome Biol Evol 7:2394–23406. CrossRefPubMedPubMedCentralGoogle Scholar
  38. Yoshida Y, Kuroiwa H et al (2010) Chloroplasts divide by contraction of a bundle of nanofilaments consisting of polyglucan. Science 329:949–953. CrossRefPubMedGoogle Scholar

Copyright information

© Springer Nature Singapore Pte Ltd. 2017

Authors and Affiliations

  • Hisayoshi Nozaki
    • 1
    Email author
  • Yu Kanesaki
    • 2
  • Motomichi Matsuzaki
    • 3
  • Shunsuke Hirooka
    • 4
    • 5
  1. 1.Department of Biological Sciences, Graduate School of ScienceUniversity of TokyoTokyoJapan
  2. 2.Research Institute of Green Science and TechnologyShizuoka UniversityShizuokaJapan
  3. 3.Department of ParasitologyNational Institute of Infectious DiseasesTokyoJapan
  4. 4.Department of Cell GeneticsNational Institute of GeneticsShizuokaJapan
  5. 5.Core Research for Evolutional Science and Technology Program, Japan Science and Technology AgencySaitamaJapan

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