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. 2021 Nov 9;2021:gigabyte32. doi: 10.46471/gigabyte.32

Bicolor angelfish (Centropyge bicolor) provides the first chromosome-level genome of the Pomacanthidae family

Chunhua Li 1,†, Xianwei Yang 1,3,†, Libin Shao 1,†, Rui Zhang 1, Qun Liu 1, Mengqi Zhang 1, Shanshan Liu 1, Shanshan Pan 1, Weizhen Xue 1, Congyan Wang 1, Chunyan Mao 1, He Zhang 1,2,*, Guangyi Fan 1,*
PMCID: PMC9650296  PMID: 36824335

Abstract

The Bicolor Angelfish, Centropyge bicolor, is a tropical coral reef fish. It is named for its striking two-color body. However, a lack of high-quality genomic data means little is known about the genome of this species. Here, we present a chromosome-level C. bicolor genome constructed using Hi-C data. The assembled genome is 650 Mbp in size, with a scaffold N50 value of 4.4 Mbp, and a contig N50 value of 114 Kbp. Protein-coding genes numbering 21,774 were annotated. Our analysis will help others to choose the most appropriate de novo genome sequencing strategy based on resources and target applications. To the best of our knowledge, this is the first chromosome-level genome for the Pomacanthidae family, which might contribute to further studies exploring coral reef fish evolution, diversity and conservation.

Data description

Background

Centropyge bicolor (NCBI:txid109723; FishbaseID: 5454; urn:lsid:marinespecies.org:taxname:211780) (Figure 1), also known as the Bicolor, Two-Colored, or Pacific Rock Beauty Angelfish, is a showy coral reef fish commonly distributed in the Indo–Pacific ocean (from East Africa to the Samoan and Phoenix Islands, north to southern Japan, south to New Caledonia; throughout Micronesia). As a member of the Pomacanthidae family, it is similar to those of the Chaetodontidae (Butterflyfishes) but is distinguished by the presence of strong preopercle spines. C. bicolor has clear boundaries between its body colors, so might be a good model in which to study body color development in coral fish [1].

Figure 1.

Figure 1.

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Photograph of Centropyge bicolor.

Context

Although the availability of genetic, and especially genomic resources, remains limited for the Pomacanthidae family, we assembled the first C. bicolor reference genome. This will provide valuable information for genetic studies of this coral reef fish, and will contribute to studies in body color diversity. With the whole genome sequence of C. bicolor, it might be possible to explore the genetic mechanisms of body color development in coral reef fish by comparative genomic methods.

Methods and results

A protocols collection for BGISEQ-500, stLFR and Hi-C library construction is available in protocols.io (Figure 2) [2].

Figure 2.

Figure 2.

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Protocols for BGISEQ-500, stLFR and Hi-C library preparation and construction, and genome assembly, for the Bicolor Angelfish, Centropyge bicolor [2]. https://www.protocols.io/widgets/doi?uri=dx.doi.org/10.17504/protocols.io.bpxhmpj6

Sample collection and genome sequencing

A C. bicolor individual was collected from the market in Xiamen, Fujian Province, China. DNA was extracted from fresh muscle tissue according to a standard protocol. Single-tube long fragment read (stLFR) [2] and Hi-C libraries were constructed following the manufacturers’ instructions [2, 3] to sequence and assemble the genome. We obtained 130.47 Gbp (gigabase pairs; ∼197×) raw stLFR data and 134.57 Gbp (∼203.20×) raw Hi-C data (Table 1) using the BGISEQ-500 platform in 100-bp (basepair) paired-end mode.

Table 1.

Statistics of DNA sequencing data.

Raw data Valid data
Libraries Read length Total bases (Gbp) Sequencing depth (×) Total bases (Gbp) Sequencing depth (×)
stLFR 100:100 130.47 197.00 60.71 91.67
Hi-C 100:100 134.57 203.20 42.51 64.19
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Sequencing depth = Total bases / Genome size, where the genome size is the result of k-mer estimation, as shown in Table 2.

Low-quality reads (sequences with more than 40% of bases with a quality score lower than 8), polymerase chain reaction (PCR) duplications, adaptor sequences and reads with a high (greater than 10%) proportion of ambiguous bases (Ns) occurring in stLFR data were filtered using SOAPnuke (v1.6.5; RRID:SCR_015025) [4]. We obtained 62.6 Gbp (∼91.67×) clean data (Table 1) to assemble the draft genome. Meanwhile, HiC-Pro (v. 2.8.0) [5] was used for the quality control of raw Hi-C data, and 42.51 Gbp (∼64.19×) valid data were used to assemble the genome to the chromosome-level (Table 1).

Genome assembly

Using GenomeScope software (RRID:SCR_017014) with stLFR clean data, k-mer distribution was used to understand the genome complexity before genome assembly [6]. The genome size of C. bicolor was estimated as 662.27 Mbp (megabase pairs), with 37.6% repeat sequences and 1.16% heterozygous sites (Table 2, Figure 3).

Table 2.

Statistical information of 17-mer analysis.

k-mer k-mer number k-mer Depth Heterozygosity (%) Genome size (Mbp)
17 50,994,645,240 77 1.16 662.27
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The genome size, G, was defined as G = Knum/Kdepth, where Knum is the total number of k-mers, and Kdepth is the most frequently occurring k-mer.

Figure 3.

Figure 3.

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The 17-mer depth distribution of Centropyge bicolor. The estimated genome size is 662.27 Mbp and the heterozygosity is 1.16%.

We reformatted the clean stLFR data into 10× Genomics format using an in-house script [7] and assembled the draft genome using Supernova (v.2.0.1, RRID:SCR_016756) [8] with default parameters. The draft genome was 681 Mbp, with a contig N50 of 115.5 Kbp (kilobase pairs) and scaffold N50 of 4.4 Mbp (Table 3), which is similar to the estimated genome size.

Table 3.

Statistics of the draft assembly with stLFR data.

Statistics Contig Scaffold
Total number (#) 40,442 29,065
Total length (bp) 655,705,062 681,285,455
Gap (N) (bp) 0 25,580,393
Average length (bp) 16,213.47 23,440.06
N50 length (bp) 115,524 4,424,004
N90 length (bp) 6,029 7,618
Maximum length (bp) 1,148,507 21,943,074
Minimum length (bp) 48 940
GC content (%) 41.74 41.74
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To obtain the chromosome-level genome, we used Juicer (v3, RRID:SCR_017226) [9] to build a contact matrix and 3dDNA (v.170123) [10] to sort and anchor scaffolds with the parameters: “–m haploid –s 4 –c 24”. There are 24 distinct contact blocks, which correspond to 24 chromosomes, representing 96% of the whole genome (Figures 4A, 5, Table 4). On evaluating the completeness of the genome and gene set using Benchmarking Universal Single-Copy Orthologs (BUSCO, v.3.0.2, RRID:SCR_015008) [11] and a vertebrata database, our assembly maintained a score of 96.2% (Table 5). We also identified putative homologous chromosomal regions between C. bicolor and Oryzias latipes by MCscanx [12] (Figure 6).

Figure 4.

Figure 4.

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Annotation of the Centropyge bicolor genome. (A) Basic genomic elements of the Centropyge bicolor genome. LTR, long terminal repeat; LINE, long interspersed nuclear elements; SINE, short interspersed elements. (B) Physical map of mitochondrial assembly.

Figure 5.

Figure 5.

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Heat map of interactive intensity between chromosome sequences.

Table 4.

Statistics of the chromosome-level genome.

Statistics Contig Scaffold
Total number (#) 40,778 28,555
Total length (bp) 655,705,062 680,873,932
Gap (N) (bp) 0 25,168,870
Average length (bp) 16,079.87 23,844.30
N50 length (bp) 113,563 21,943,074
N90 length (bp) 5,988 7,542
Maximum length (bp) 1,148,507 28,105,280
Minimum length (bp) 43 43
GC content (%) 41.74 41.74
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Table 5.

Statistics of the BUSCO assessment.

Types of BUSCOs Gene set Assembly
Number Percentage (%) Number Percentage (%)
Complete BUSCOs 2,408 93.1 2,486 96.2
Complete single-copy BUSCOs 2,348 90.8 2,438 94.3
Fragmented BUSCOs 81 3.1 64 2.5
Missing BUSCOs 97 3.8 36 1.3
Total BUSCO groups searched 2,586 100 2,586 100
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Figure 6.

Figure 6.

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Homologous chromosomal regions between Centropyge bicolor and Oryzias latipes.

In addition, we cut off partial stLFR reads (25 M) for assembly by MitoZ with default parameters [13] and obtained a 16,961-bp circular mitochondrial genome of C. bicolor. Thirteen protein-coding genes, 24 tRNA genes and three rRNA genes were annotated by GeSeq (RRID:SCR_017336) [14] (Figure 4B).

Genomic annotation

For the annotation of repeats, we carried out homolog annotation and ab initio prediction independently. RepeatMasker (v.4.0.6, RRID:SCR_012954) [15], RepeatProteinMask (a module from RepeatMasker) and trf (Tandem Repeats Finder, v.4.07b) [16] were used to identify known repetitive sequences by comparing the whole genome with RepBase [17]. LTR_FINDER (v.1.06, RRID:SCR_015247) [16, 18] and RepeatModeler (v.1.0.8, RRID:SCR_015027) [19] were used in de novo prediction. We also classified transposable elements (TEs) from the integration of all repeats. In total, we identified 124 Mbp (18.32% of the entire genome) of repetitive sequences (Figure 4A, Table 6), including 110 Mbp of TEs (Figure 4A, Table 7).

Table 6.

Statistics of repetitive sequences.

Type Repeat size (bp) Percentage of genome (%)
TRF 14,165,095 2.08
RepeatMasker 43,423,877 6.38
RepeatProteinMask 12,503,750 1.84
De novo 110,871,693 16.28
Total 124,708,977 18.32
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Table 7.

Statistics of transposable elements.

Repbase TEs, n (%) Protein TEs, n (%) De novo TEs, n (%) Combined TEs, n (%)
DNA 27,163,851 (3.990) 1,068,990 (0.157) 61,731,447 (9.067) 70,925,963 (10.417)
LINE 10,228,332 (1.502) 6,956,340 (1.022) 20,006,579 (2.938) 26,714,285 (3.924)
SINE 856,125 (0.126) 0 (0.000) 497,024 (0.073) 1,187,676 (0.174)
LTR 10,971,817 (1.611) 4,485,808 (0.659) 16,270,071 (2.390) 23,101,529 (3.393)
Other 10,041 (0.001) 0 0 10,041 (0.001)
Unknown 0 0 14,054,230 (2.064) 14,054,230 (2.064)
Total 43,423,877 (6.378) 12,503,750 (1.836) 99,265,690 (14.579) 109,868,166 (16.136)
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Homolog-based and ab initio prediction were used to identify the protein-coding genes. Augustus (v.3.3, RRID:SCR_008417) [20] was used in ab initio prediction basing on a repeat-masked genome [21]. Protein sequences of Astatotilapia calliptera, Danio rerio, Larimichthys crocea, and Oreochromis niloticus were downloaded from the National Center for Biotechnology Information (NCBI) GenBank database and aligned to the C. bicolor genome for homolog gene annotation with Genewise (v2.4.1, RRID:SCR_015054) [22]. Finally, we used GLEAN [23] to integrate all the above evidence and obtained a total of 21,774 genes, which contained 11 exons on average and had an average coding sequence (CDS) length of 1,575 bp (Table 8).

Table 8.

Statistics of the predicted genes in the bicolor angelfish genome.

Gene set Gene number Average transcript length (bp) Average CDS length (bp) Average intron length (bp) Average exon length (bp) Average exons per gene
Homolog Astatotilapia calliptera 51,174 21,762.29 2,259.23 1,691.33 180.29 12.53
Danio rerio 22,005 27,982.75 1,570.36 3,438.82 180.90 8.68
Larimichthys crocea 47,419 19,884.78 2,139.39 1,575.94 174.50 12.26
Oreochromis niloticus 47,067 17,771.04 1,906.97 1,608.29 175.53 10.86
De novo Augustus 34,470 9,675.42 1,335.20 1,344.81 185.40 7.20
GLEAN 21,774 14,024.40 1,906.28 1,206.07 172.55 11.05
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The GLEAN gene set is the integrated result of de novo gene predictions and homolog gene predictions.

To predict gene functions, 21,774 genes were aligned against several public databases, including TrEMBL [24], SwissProt [24], KEGGViewer [25] and InterProScan [26]. As a result, 99.67% of all genes were predicted functionally (Table 9, Figure 7).

Table 9.

Statistics of the functional annotation.

Database Number Percentage (%)
Total 21,774 100.00
SwissProt 20,784 95.45
KEGG 19,168 88.03
TrEMBL 21,688 99.61
Interpro 20,153 92.56
Overall 21,702 99.67
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Figure 7.

Figure 7.

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Venn diagram of orthologous gene families. Four teleost species (Centropyge. bicolor, Larimichthys crocea, Oreochromis niloticus, and Danio rerio) were used to generate the Venn diagram based on gene family cluster analysis.

Phylogenetic analysis

We downloaded the gene data of seven representative teleost fishes from NCBI to study the phylogenetic relationships between C. bicolor. These seven fishes were: Danio rerio, Gasterosteus aculeatus, Gadus morhua, Larimichthys crocea, Oryzias latipes, Oreochromis niloticus and Tetraodon nigroviridis. For each dataset, the longest transcripts were selected and aligned to each other by BLASTP (v2.9.0, RRID:SCR_001010) [27] (E-value ≤ 1e-5). TreeFam (v.2.0.9, RRID:SCR _013401) [28] was used to cluster gene families, with default parameters. Among all 20,706 clustered gene families, there were 4,450 common single-copy families and 57 families specific to C. bicolor (Table 10). With single-copy sequences, we used PhyML (v.3.3, RRID:SCR_014629) [29] to construct the phylogenetic tree of C. bicolor and the seven other fishes mentioned above, setting D. rerio as an outgroup.

Table 10.

Statistics of gene family clustering.

Species Total genes Unclustered genes Families Unique families Average number of genes per family
Centropyge bicolor 21,774 694 16,219 57 1.3
Danio rerio 30,067 2,188 18,575 726 1.5
Gasterosteus aculeatus 20,756 784 15,921 16 1.25
Gadus morhua 19,987 535 15,630 9 1.24
Larimichthys crocea 24,403 610 17,273 55 1.38
Oryzias latipes 19,535 1,048 14,805 87 1.25
Oreochromis niloticus 21,431 180 15,780 14 1.35
Tetraodon nigroviridis 19,544 901 14,803 57 1.26
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Based on the phylogenetic tree and single-copy sequences, the divergence time between different species was estimated by MCMCTREE with parameters of “–model 0 –rootage 500 -clock 3”. The results showed that C. bicolor was formed ∼34.95 million years ago, when differentiated from the common ancestor with L. crocea (Figure 8).

Figure 8.

Figure 8.

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Comparative analysis of the Centropyge bicolor genome. (A) The protein-coding genes of the eight species were clustered into 17,849 gene families. Among these gene families, 4,450 were single-copy gene families. (B) Phylogenetic analysis of Centropyge bicolor (Cbi.), Danio rerio (Dre.), Gasterosteus aculeatus (Gac.), Gadus morhua (Gmo.), Larimichthys crocea (Lcr.), Oryzias latipes (Ola.), Oreochromis niloticus (Oni.), and Tetraodon nigroviridis (Tni.) using single-copy gene families. The species differentiation time between Centropyge bicolor and Larimichthys crocea was ∼34.95 million years.

Analysis of bicolor formation in teleosts

Current studies suggest that different pigment cells produce different pigments. Some types of pigment cells already have been identified in teleost [30]. C. bicolor has an attractive body color with clear color boundaries, but the molecular mechanism underlying this remains unknown. Compared with other teleost, there are 1,081 expanded gene families and 57 specific gene families in C. bicolor (Figure 9). Functional enrichment analysis showed that notable expansion occurred in those gene families related to visual development and enzyme metabolism (Figure 9).

Figure 9.

Figure 9.

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Statistics of gene function enrichment (Gene Ontology) for expanded genes of Centropyge bicolor. Nodes are colored by q-value (adjusted p-value). Node size is shown according to its enriched gene number.

Re-use potential

Coral reef fishes, with distinctive color patterns and color morphs, are important for understanding the adaptive evolution of fishes. In this study, we firstly assembled a high-quality, chromosome-level genome of C. bicolor, with a length of 681 Mbp, and annotated 21,774 genes. This is the first genome of a fish from the Pomacanthidae family. These genomic data will be useful for genome-scale comparisons and further studies on the mechanisms underlying colorful body development and adaptation.

Acknowledgements

We thank the China National Genebank for technical support in constructing and sequencing the stLFR library.

Funding Statement

This work was supported by funding from the “Blue Granary” project for scientific and technological innovation of China (2018YFD0900301-05).

Data availability

The data sets supporting the results of this article are available in the GigaScience Database [31]. Raw reads from genome sequencing and assembly are deposited at the China National Gene Bank under reference number CNP0001160, which contains sample information (CNS0315939), Hi-C raw data (CNX0286336) and stLFR raw data (CNX0286337). The project also has been deposited at NCBI under accession ID PRJNA702283.

Declarations

List of abbreviations

bp: base pair; BUSCO: Benchmarking Universal Single-Copy Orthologs; Gbp: gigabase pair; Kbp: kilobase pair; KEGG: Kyoto Enyclopedia of Genes and Genomes; Mbp: megabase pair; NCBI: National Center for Biotechnology Information; stLFR: single-tube long fragment reads; TE: transposable element.

Ethical approval

All resources used in this study were approved by the Institutional Review Board of BGI (IRB approval No. FT17007). This experiment has passed the ethics audit of the Beijing Genomics Institute (BGI) Gene Bioethics and Biosecurity Review Committee.

Consent for publication

Not applicable.

Competing interests

The authors declare that they have no competing interests.

Funding

This work was supported by funding from the “Blue Granary” project for scientific and technological innovation of China (2018YFD0900301-05).

Authors’ contributions

H.Z. and G.F. designed this project. M.Z. prepared the samples. S.L., S.P., W.X., C.W. and C.M. conducted the experiments. C.L., X.Y., L.S., R.Z. and Q.L. did the analyses. C.L., X.Y., L.S., R.Z. wrote and revised the manuscript. All authors read and approved the final version of the manuscript.

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Is the language of sufficient quality? No
Please add additional comments on language quality to clarify if needed Almost every second sentence in the abstract would need work, and so is the rest of the manuscript.
Are all data available and do they match the descriptions in the paper? Yes
Additional Comments
Are the data and metadata consistent with relevant minimum information or reporting standards? See GigaDB checklists for examples <a href="http://gigadb.org/site/guide" target="_blank">http://gigadb.org/site/guide</a> Yes
Additional Comments
Is the data acquisition clear, complete and methodologically sound? Yes
Additional Comments
Is there sufficient detail in the methods and data-processing steps to allow reproduction? Yes
Additional Comments
Is there sufficient data validation and statistical analyses of data quality? Yes
Additional Comments
Is the validation suitable for this type of data? Yes
Additional Comments
Is there sufficient information for others to reuse this dataset or integrate it with other data? Yes
Additional Comments General comments: The authors have created a chromosome-level genome assembly of bicolor angelfish using stLFR and HiC libraries. The language in this manuscript needs some work. After commenting on every second sentence in the abstract regarding some language matter, I saw that I couldn’t continue commenting all these matters. Please do a good clean-up in the language, so that it is easier to read. I’ll point out some issues during the manuscript, but will not find all and I can’t manage to point out all I do find. Specific comments: Line 19: «...special and beautiful two-color body” is a bit subjective. Maybe something like “…remarkable and striking two-color body” instead? Line 20: I know this is the abstract, but I don’t understand what “the mechanism of bicolor body” could mean. Maybe rephrase? Line 22: I’ve seen this many places, but it should be a lower-case k in kb, not upper case like Kb. The k stands for kilo which is a metric prefix meaning thousand (https://en.wikipedia.org/wiki/Metric_prefix). Line 25: “As we are known,” should be “as far as we know”. Line 27: “Future research” instead of “future researches”. Line 46: Which protocol are you talking about? Table 1: How can you end up with more “valid data” than “raw data”? Did you mix up something here? It looks consistent with the text, but there’s likely something wrong.
Any Additional Overall Comments to the Author
Recommendation Minor Revision
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GigaByte.

Review MS

Editor: Claudius F Kratochwil
Reviewer name and names of any other individual's who aided in reviewer Claudius Kratochwil
Do you understand and agree to our policy of having open and named reviews, and having your review included with the published papers. (If no, please inform the editor that you cannot review this manuscript.) Yes
Is the language of sufficient quality? No
Please add additional comments on language quality to clarify if needed The text is understandable, but has many grammatical errors. The manuscript would greatly improve through language editing.
Are all data available and do they match the descriptions in the paper? Yes
Additional Comments I did not check every single file, but all data I looked for I found to be publicly available. It would help if the "Availability of supporting data and materials" statement would be a bit more comprehensive. Data A is deposited under X, Data B is deposited under Y-Z instead of just providing the project ID.
Are the data and metadata consistent with relevant minimum information or reporting standards? See GigaDB checklists for examples <a href="http://gigadb.org/site/guide" target="_blank">http://gigadb.org/site/guide</a> Yes
Additional Comments To the best of my knowledge. Not my area of expertise.
Is the data acquisition clear, complete and methodologically sound? No
Additional Comments I was lacking information about the transcriptomic data (it says in line 44 that RNA was extracted) that was used for the annotation? Was RNA only extracted from the muscle? Maybe the caveats that go along with that should be discussed. How was the data processed? How many reads etc. I think the manuscript lacks information about this unless I misunderstood where the data for the "transcript-based prediction" came from. Then this should be indicated more clearly.
Is there sufficient detail in the methods and data-processing steps to allow reproduction? Yes
Additional Comments To the best of my knowledge. I am not an expert on this. Minor comments: l 46: Which protocol?
Is there sufficient data validation and statistical analyses of data quality? Not my area of expertise
Additional Comments One thing that could be probably additionally done is to provide dot plots with the 1-2 more closely related species with chromosome level assemblies (probably Tilapia or Medaka).
Is the validation suitable for this type of data? Yes
Additional Comments As far as I can judge the analysis is fine.
Is there sufficient information for others to reuse this dataset or integrate it with other data? Yes
Additional Comments Genome and annotation are available, which is the most important for reuse and integration with other data sets. So as far as I can judge there is sufficient information for others.
Any Additional Overall Comments to the Author From my viewpoint, this is a useful chromosome-level genome, so I support its publication. Beyond being a useful resource, I was however a bit disappointed by the 'scientific part' regarding the bi-color body formation. While the pigmentation of the bicolor angelfish is certainly a very exciting phenotype, the analysis performed is far too superficial to give any solid insights into the phenotype. I would suggest the authors toning this down in title, abstract and main text. It is fine to mention this as a future research direction and to state that the performed initial analysis (fig. 6 and 7) might aid these investigations, but the data does not permit further conclusions. Especially as GigaByte does not focus on analyses for biological findings, this should be completely sufficient.
Recommendation Major Revision
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GigaByte.

Editor Decision

Editor: Hongfang Zhang
GigaByte. 2021 Nov 9;2021:gigabyte32.

Major Revision

Chunhua Li
GigaByte.

Assess Revision

Editor: Hongfang Zhang
GigaByte.

Re-Review MS

Editor: Claudius F Kratochwil
Comments on revised manuscript I am happy with the changes made and thank the authors for addressing them. The manuscript is in my opinion acceptable for publication. Congratulations to the authors for providing a reference genome for this exciting fish species to the community.
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GigaByte.

Editor Decision

Editor: Hongfang Zhang
GigaByte.

Final Data Preparation

Editor: Mary-Ann Tuli
GigaByte.

Editor Decision

Editor: Hongfang Zhang
GigaByte.

Accept

Editor: Scott Edmunds
Comments to the Author Thanks for your great submission. You will receive the proofs shortly.
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Export to Production

Editor: Scott Edmunds

Associated Data

    This section collects any data citations, data availability statements, or supplementary materials included in this article.

    Data Availability Statement

    The data sets supporting the results of this article are available in the GigaScience Database [31]. Raw reads from genome sequencing and assembly are deposited at the China National Gene Bank under reference number CNP0001160, which contains sample information (CNS0315939), Hi-C raw data (CNX0286336) and stLFR raw data (CNX0286337). The project also has been deposited at NCBI under accession ID PRJNA702283.

    Articles from GigaByte are provided here courtesy of Gigascience Press

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