- Research article
- Open Access
A 100%-complete sequence reveals unusually simple genomic features in the hot-spring red alga Cyanidioschyzon merolae
- Hisayoshi Nozaki1Email author,
- Hiroyoshi Takano2,
- Osami Misumi3, 4,
- Kimihiro Terasawa5, 6,
- Motomichi Matsuzaki1,
- Shinichiro Maruyama1, 6,
- Keiji Nishida3, 4,
- Fumi Yagisawa3, 4,
- Yamato Yoshida7, 4,
- Takayuki Fujiwara3, 4,
- Susumu Takio8,
- Katsunori Tamura6,
- Sung Jin Chung2, 10,
- Soichi Nakamura9,
- Haruko Kuroiwa3, 4,
- Kan Tanaka6,
- Naoki Sato5 and
- Tsuneyoshi Kuroiwa3, 4
© Nozaki et al; licensee BioMed Central Ltd. 2007
Received: 31 January 2007
Accepted: 10 July 2007
Published: 10 July 2007
All previously reported eukaryotic nuclear genome sequences have been incomplete, especially in highly repeated units and chromosomal ends. Because repetitive DNA is important for many aspects of biology, complete chromosomal structures are fundamental for understanding eukaryotic cells. Our earlier, nearly complete genome sequence of the hot-spring red alga Cyanidioschyzon merolae revealed several unique features, including just three ribosomal DNA copies, very few introns, and a small total number of genes. However, because the exact structures of certain functionally important repeated elements remained ambiguous, that sequence was not complete. Obviously, those ambiguities needed to be resolved before the unique features of the C. merolae genome could be summarized, and the ambiguities could only be resolved by completing the sequence. Therefore, we aimed to complete all previous gaps and sequence all remaining chromosomal ends, and now report the first nuclear-genome sequence for any eukaryote that is 100% complete.
Our present complete sequence consists of 16546747 nucleotides covering 100% of the 20 linear chromosomes from telomere to telomere, representing the simple and unique chromosomal structures of the eukaryotic cell. We have unambiguously established that the C. merolae genome contains the smallest known histone-gene cluster, a unique telomeric repeat for all chromosomal ends, and an extremely low number of transposons.
By virtue of these attributes and others that we had discovered previously, C. merolae appears to have the simplest nuclear genome of the non-symbiotic eukaryotes. These unusually simple genomic features in the 100% complete genome sequence of C. merolae are extremely useful for further studies of eukaryotic cells.
The biological sciences have been embracing a new paradigm as a result of accruing genome information [1–13]. However, all previously reported eukaryotic nuclear genome sequences have been incomplete, especially in highly repeated units and chromosomal ends. Because repetitive DNA is essential to genome function , and may contribute to the diversity of isoforms  and the evolution of life , complete chromosomal structures are fundamental for understanding eukaryotic cells.
Our recently published nuclear-genome sequence of the ultra-small, hot-spring red alga, Cyanidioschyzon merolae 10D, revealed some unique features, such as very few introns, only three copies of ribosomal (r)DNA, and a small total number of genes [9, 10]. However, because uncertainties remained regarding the features of certain important repeated elements, such as histone-gene clusters and telomeres , this sequence, like all previous eukaryotic nuclear-genome sequences, was incomplete. Given the functional significance of such elements , it was obviously desirable to complete the sequence and resolve all ambiguities before attempting to summarize all of the unique features of the C. merolae genome. Therefore, we aimed to complete all previous gaps and sequenced all the remaining chromosomal ends, to construct the first nuclear genome sequence that is 100% complete. The results demonstrated that C. merolae possesses the simplest nuclear genome known among non-symbiotic eukaryotes.
Results and Discussion
A 100%-complete genome sequence
Key features of the 22 chromosomes constituting the three genomes of the hot-spring red alga Cyanidioschyzon merolae 10D
No. of nucleotides(bp)
Shape of chromosome
No. of protein-coding genes
1 232 258
1 253 087
1 282 939
1 621 617
16 546 747
Total of 3 genomes
16 728 945
Telomeres and subtelomeric regions
Whole-genome shotgun sequencing suggested that the repeat unit in C. merolae telomeres is AATGGGGGG , but in that study only six of the 40 chromosome ends were examined  (Figure 1). Here the sequencing of all remaining termini confirmed that AATGGGGGG is the telomere repeat sequence in all C. merolae chromosomal ends. In most plants, the telomeres are composed of many copies of the sequence TTTAGGG , and the C. merolae telomere sequence, AATGGGGGG, has never yet been found elsewhere.
Telomere length varies among plants from approximately 0.5 kbp in the green alga Chlorella vulgaris to 150 kbp in tobacco [22, 23]. Telomere restriction fragment analyses using the (CCCCCCATT)3 probe revealed AATGGGGGG repeats varying from 400 to 700 bp in the total chromosomal ends in the C. merolae genome (data not shown). Our Southern blot analysis using a specific genomic probe suggested that C. merolae chromosome 15 has around a 400-bp telomere repeat sequence at the left end (see Additional file 3). However, the longest telomeric repeats that could be sequenced in this study were 2.5 repeats (AATGGGGGGAATGGGGGGAATGGG) in the right end of chromosome 1, possibly because long stretches of AATGGGGGG repeats are difficult to clone or sequence using conventional techniques used in this and previous studies .
The putative telomerase catalytic subunit, telomerase reverse transcriptase (TERT) is transcribed (CMD110C) in C. merolae . In the C. merolae genome, we found two possible telomerase RNA subunit genes in chromosomes 13 and 16, based on two transcripts, CMM123T and CMP131T, which included UUCCCCCCAUU and CCAUUCCCCCCAUU sequences, respectively. The telomerase RNA template sequence (CCCCCCAUU) has been detected in only these two hypothetical non-coding RNA genes among all the predicted genes in the present 100% complete nuclear genome. These are the first convincing candidate telomerase-RNA subunit genes in plant and algal lineages.
Comparison of the nuclear genomes of Cyanidioschyzon, Ostreococcus (an ultra-small green alga), Arabidopsis (a flowering plant) and Ashbya (a filamentous fungal pathogen).
No. of protein-coding genes
Genes with introns (%)
No. of rRNA gene units
No. of chromosomes with histone genes
Transposable elements in genome (%)
Telomere repeat sequences
In contrast to this, 253 copies of a novel interspersed repetitive element were found in the C. merolae genome. All copies have a truncated ORF that is weakly related (BLASTX E-value = 10-5-4 × 10-2) to a putative protein, WSV486, that is encoded in the genome of the shrimp spot syndrome virus . These repetitive elements have an average size of 3.2 kbp, are distributed randomly on all chromosomes, and altogether comprise about 5% of the genome. Because these elements exhibit transcriptional activity , they may contribute to genomic or cellular functions in C. merolae in the same manner as repetitive DNA does in other eukaryotes .
The smallest known histone-gene cluster, a unique telomeric repeat, a very low density of transposable elements, and other previously described simple features of the C. merolae nuclear genome [9, 10] (Table 2) are very distinctive, and constitute the simplest set of genomic features found in any non-symbiotic eukaryote yet studied. Such simple features are generally considered to result from consequences of reductive evolution of an ultra-small eukaryote . However, none of these features is shared by the similarly ultra-small green alga, Ostreococcus, in which 39% of the genes contain introns, histone genes are dispersed across at least six chromosomes, and 417 transposable elements and 8166 protein-coding genes are distributed among the chromosomes  (see Table 2). These may suggest differences in modes of genome reduction between ancestors of Cyanidioschyzon (red algae) and Ostreococcus (green plants). On the other hand, algae living in acidic hot springs (pH 1.5, 45°C) might be candidates for retaining ancient plant attributes, because the volcano activity is thought to have been providing such an extreme environment throughout Earth's history. Very recently, Cunningham et al  reported that C. merolae contains perhaps the simplest assortment of chlorophylls and carotenoids found in any eukaryotic photosynthetic organism. In addition, the C. merolae plastid genome contains a large number of genes, which is thought to be a primitive feature, because reversal of plastid-gene loss is generally considered to be impossible [34, 35]. Thus, our hypothesis is that some of the unusual or simple genomic characteristics of C. merolae may represent primitive features that have been conserved in Cyanidioschyzon, but have become extensively modified during the evolution of other plant lineages. Alternatively, the unique genomic features of C. merolae (Table 2) may reflect adaptation to the extreme environment. However, genome information for other hot-spring red algae is very limited. The recently released nuclear genome sequence of another hot-spring red alga Galdieria has not revealed the chromosomal structures of its components, such as rDNA units or histone cluster area. . Further information on the complete nuclear genomes of other plants, including other hot-spring red algae, red macro-algae, and other members of plant and algal lineages, will be needed to determine whether C. merolae actually has primitive genomic features.
Three kinds of genomes are found in many eukaryotic cells: nuclear, mitochondrial, and plastid . Based on the present nuclear genome data and the previously published mitochondrial and plastid genome sequences [18, 19], all major types of eukaryotic genetic information are present in C. merolae. In addition, as revealed by the present 100% complete genome, C. merolae contains unusually simple sets of genes and sequences (Table 2). For example, because almost all protein-coding nuclear genes of C. merolae lack introns (Table 2), the complete sequence of the genome provided here can be used directly to deduce the sequences of all of its proteins, which will make it extremely valuable for future proteomics research. Therefore, C. merolae represents an ideal model organism for studying the fundamental relationships among the chloroplast, mitochondrial and nuclear of genomes. The complete nuclear genome sequence reported here will greatly improve the precision of biological analyses of C. merolae, including studies of chromosome structure and gene structure/annotation. Furthermore, because C. merolae inhabits hot springs (45°C) , most of its proteins must be unusually heat-stable, and so its proteome may well provide important new insights into the structural basis for heat stability of proteins.
Filling gaps between contigs/fragments
Previously constructed C. merolae BAC clones  were used for filling in previously existing gaps between contigs. PCRs of BAC clones containing unsequenced regions were carried out using Taq polymerase with GC buffer (Takara LA Taq; Takara Bio Inc., Osaka, Japan) and specific primers complementary to sequences flanking the gaps. DNA walking annealing control primer technology (DNA Walking SpeedUp™ Kit; Seegene, Seoul, Korea) was also used to directly amplify unknown sequences adjacent to known sequences within a contig. PCR products were sequenced by cycle sequencing (Big-Dye Terminator Cycle Sequencing Kit v 3.1; Applied Biosystems, Foster City, CA, USA), except for a single gap in chromosome 10, which was filled by a sequencing reaction performed using in vitro transcription (CUGA Sequencing Kit; Nippon Genetech Co., Ltd., Tokyo, Japan).
Sequencing of each chromosomal end
Assembling sequence data and gene annotation
Assembling of sequence data and two strategies for gene prediction have been described previously .
Complete determination of the histone cluster area
To determine the complete sequences of the histone cluster area in the C. merolae genome, we carried out NotI and ApaI subcloning of the BAC clone GESZ2-b20, which included possible histone clusters in chromosome 14 . Restriction-enzyme analysis, Southern blot analysis with histone-related probes and end sequencing of the subclones revealed relative positions of the subclones on chromosome 14 (Figure 2). Six gaps between contigs/fragments in the histone cluster area  were filled using primer walking of the subclones. For details, see Additional files 1 and 4.
The 100% chromosome sequences are accessible under the DDBJ with accession numbers AP006483–AP006502 (chromosome 1–20). Sequences and annotation are available at http://merolae.biol.s.u-tokyo.ac.jp/.
We thank Professor D. L. Kirk (Washington University) for critically reading the manuscript. This work was supported by Grant-in-Aid for Creative Scientific Research (No. 16GS0304 to KanT, NS and HN) and Grant-in-Aid for Scientific Research (No. 17370087 to HN), from the Ministry of Education, Culture, Sports, Science and Technology of Japan; and by grants from Frontier Project "Adaptation and Evolution of Extremophile" (to TK) from the Ministry of Education, Culture, Sports, Science and Technology of Japan, and from the Program for the Promotion of Basic Research Activities for Innovative Biosciences (PROBRAIN to TK).
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