Abstract
We present a genome assembly for Cottoperca gobio (channel bull blenny, (Günther, 1861)); Chordata; Actinopterygii (ray-finned fishes), a temperate water outgroup for Antarctic Notothenioids. The size of the genome assembly is 609 megabases, with the majority of the assembly scaffolded into 24 chromosomal pseudomolecules. Gene annotation on Ensembl of this assembly has identified 21,662 coding genes.
Keywords: Cottoperca gobio, channel bull blenny, genome assembly chromosomal, Notothenioidei
Species taxonomy
Eukaryota; Metazoa; Chordata; Vertebrata; Gnathostomata; Actinopterygii; Teleostei; Clupeocephala; Percomorphaceae; Perciformes; Notothenioidei; Bovichtidae; Cottoperca; Cottoperca gobio (Günther, 1861) - synonym: Cottoperca trigloides ( Balushkin, 2000), NCBI taxid: 56716.
Background
Cottoperca gobio (channel bull blenny) is a member of the Bovichtidae family of the Notothenioidei, a fish group endemic to the Southern Ocean. The Bovichtidae (thornfishes), are considered to be the most basally diverging family of notothenioids and are less adapted to life in the extreme cold in comparison to Antarctic members of the clade ( Near et al., 2015). C. gobio occupies the Patagonian regions of Chile and Argentina, and the area around the Falkland Islands. In contrast to Antarctic notothenioids (cryonotothenioids), the Bovichtidae do not produce antifreeze glycoproteins (AFGPs), a key adaptation to extreme Antarctic cold ( Chen et al., 1997; Cheng et al., 2003) and their hemoglobins possess slightly higher oxygen affinity than most high-Antarctic species ( Giordano et al., 2006; Giordano et al., 2009). Cytogenetic investigation of C. gobio showed that the karyotype of this species consists of 2n=48 chromosomes ( Pisano et al., 1995). This condition, shared by other Bovichtidae, is considered to be the ancestral karyotype condition for all notothenioids ( Mazzei et al., 2006).
Here, we present a chromosomally complete genome sequence of Cottoperca gobio generated using specimens collected south of the Falkland Islands/Islas Malvinas. We trust that this genome sequence will be used to aid analysis of population structure and phylogeography of non-Antarctic and Antarctic notothenioid fish species, which are increasingly under threat due to climate change and human activities ( Dornburg et al., 2017).
Genome sequence report
The C. gobio genome was sequenced from a specimen collected under permits to fish in territorial waters of the Falkland Islands/Islas Malvinas issued by the United Kingdom, by the Falkland Islands Government, and by Argentina. The genome assembly for C. gobio (fCotGob3.1) is based on a combination of data from four technologies, including 75x coverage Pacific Biosciences (PacBio) single-molecule long reads (N50 14 kb), 54x coverage of Illumina data generated from a 10X Genomics Chromium library (estimated molecule length N50 43 kb), and BioNano Saphyr two-enzyme data (BspQI and BssSI). Additionally, 145x coverage of Illumina HiSeqX data were obtained from a Hi-C library prepared by Arima Genomics using tissue from a second individual (fCotGob2, spleen tissue).
The final assembly has a total length of 609 Mb, in 322 sequence scaffolds with a scaffold N50 of 25 Mb ( Figure 1; Table 1). The majority (94.36%) of the assembly sequence was assigned to 24 chromosomal-level scaffolds using the Hi-C data ( Figure 2; Table 2). The assembly has a BUSCO ( Simão et al., 2015) gene completeness score of 93.4% using the actinopterygii reference set (with -sp zebrafish parameter). The chromosomes clearly show a one-to-one relationship with those in the Japanese medaka ( Oryzias latipes) HdrR assembly GCA_002234675.1 ( Figure 3 and Figure 4), with 3671 of the 3780 complete and single copy BUSCO genes present in both genomes found on homologous chromosomes (97.1%), and were thus named correspondingly. Analysis of conserved syntenies detected no major interchromosomal rearrangements in the approximately 195 million years since the divergence of medaka and C. gobio lineages ( Steinke et al., 2006), but many intrachromosomal rearrangements ( Figure 4). While not fully phased, the assembly deposited represents one haplotype. Contigs corresponding to the second haplotype have also been deposited.
Figure 1. Genome assembly of Cottoperca gobio, fCotGob3.1. - BlobToolKit Snailplot, showing N50 metrics and BUSCO gene completeness.
BlobToolKit plots are available at: fCotGob3.1 - BlobToolKit.
Table 1. Data information for Cottoperca gobio, fCotGob3.1 genome assembly.
| Project accession information | |
|---|---|
| Assembly identifier | fCotGob3.1 |
| Species | Cottoperca gobio ( Cottoperca trigloides) |
| Specimens | fCotGob3 (PacBio, 10XG and BioNano),
fCotGob2 (Hi-C and RNA-seq) |
| fCotGob1 (RNA-seq) | |
| NCBI taxonomy ID | 56716 |
| BioProject | PRJEB30272 |
| Study accession | PRJEB19273 |
| BioSample IDs | SAMEA104132835 (fCotGob1)
SAMEA5365137 (fCotGob1.brain1) SAMEA5365124 (fCotGob1.gonad1) SAMEA5365123 (fCotGob1.muscle1) SAMEA104242971 (fCotGob2) SAMEA4872137 (fCotGob2.spleen1) SAMEA104242975 (fCotGob3) |
| Raw data accessions | |
| Pacific Biosciences SEQUEL I | ERR2219167 - ERR2219176 |
| 10X Genomics Illumina | ERR2639757 - ERR2639760 |
| Hi-C Illumina | ERR4179340 - ERR4179344 |
| BioNano | ERZ1392783 - ERZ1392785 |
| RNA-seq | ERR3132340 (fCotGob1.brain1)
ERR3132342 (fCotGob1.gonad1) ERR3132341 (fCotGob1.muscle1) ERR2639616 (fCotGob2.spleen1) |
| Genome assembly | |
| Assembly accession | GCA_900634415.1 |
| Accession of alternate haplotype | GCA_900634435.1 |
| Span (Mb) | 609 |
| Number of contigs | 766 |
| Contig N50 length (Mb) | 5,939,854 |
| Number of scaffolds | 322 |
| Scaffold N50 length (Mb) | 25,156,145 |
| Longest scaffold (Mb) | 30.48 |
| BUSCO genome score | C:93.4%, [S:90.5%, D:2.9%], F:1.3%, M:5.3%, n:4584 |
Figure 2. Hi-C contact map for the genome assembly of Cottoperca gobio, fCotGob3.1.
Visualized in Juicebox ( Durand et al., 2016).
Table 2. Chromosomal pseudomolecules in the genome assembly fCotGob3.1, of species Cottoperca gobio - GCA_900634415.1.
| Name | INSDC | RefSeq | Size (Mb) | GC% | Protein | Gene |
|---|---|---|---|---|---|---|
| 1 | LR131916.1 | NC_041355.1 | 27.06 | 40.8 | 1,808 | 1,175 |
| 2 | LR131927.1 | NC_041356.1 | 12.92 | 41.9 | 792 | 681 |
| 3 | LR131933.1 | NC_041357.1 | 30.03 | 40.3 | 1,487 | 919 |
| 4 | LR131934.1 | NC_041358.1 | 28.95 | 40.7 | 1,629 | 1,007 |
| 5 | LR131935.1 | NC_041359.1 | 30.48 | 40.9 | 2,033 | 1,302 |
| 6 | LR131936.1 | NC_041360.1 | 27.68 | 40.9 | 1,823 | 1,143 |
| 7 | LR131937.1 | NC_041361.1 | 23.07 | 41 | 1,619 | 1,088 |
| 8 | LR131938.1 | NC_041362.1 | 23.43 | 41.2 | 1,836 | 1,194 |
| 9 | LR131939.1 | NC_041363.1 | 30.07 | 41 | 1,888 | 1,158 |
| 10 | LR131917.1 | NC_041364.1 | 27.44 | 40.8 | 1,407 | 992 |
| 11 | LR131918.1 | NC_041365.1 | 22.19 | 40.8 | 1,440 | 909 |
| 12 | LR131919.1 | NC_041366.1 | 22.9 | 40.6 | 1,424 | 850 |
| 13 | LR131920.1 | NC_041367.1 | 27.74 | 41 | 1,542 | 1,029 |
| 14 | LR131921.1 | NC_041368.1 | 25.7 | 40.6 | 1,627 | 1,134 |
| 15 | LR131922.1 | NC_041369.1 | 24.96 | 41 | 1,365 | 967 |
| 16 | LR131923.1 | NC_041370.1 | 26.58 | 41 | 1,811 | 1,094 |
| 17 | LR131924.1 | NC_041371.1 | 25.16 | 40.8 | 1,663 | 1,228 |
| 18 | LR131925.1 | NC_041372.1 | 14.93 | 41.8 | 1,018 | 690 |
| 19 | LR131926.1 | NC_041373.1 | 21.06 | 41.2 | 1,563 | 969 |
| 20 | LR131928.1 | NC_041374.1 | 17.6 | 41.4 | 964 | 649 |
| 21 | LR131929.1 | NC_041375.1 | 24.1 | 40.6 | 1,400 | 937 |
| 22 | LR131930.1 | NC_041376.1 | 22.61 | 41.3 | 1,415 | 1,026 |
| 23 | LR131931.1 | NC_041377.1 | 15.93 | 41.9 | 973 | 594 |
| 24 | LR131932.1 | NC_041378.1 | 22.44 | 41.1 | 1,229 | 1,184 |
| Unplaced | - | . | 34.34 | 41.6 | 2,093 | 1,676 |
Figure 3. Syntenic relationships of fCotGob3.1 assembly with Japanese medaka HdrR chromosomes, based on single copy orthologs.
Visualised in Circos ( Krzywinski et al., 2009).
Figure 4. Examples of conserved synteny between Japanese medaka HdrR (purple) and fCotGob3.1 (pink) from chromosomes 1, 3, 6, and 16 (source: Ensembl).
Gene annotation
An Ensembl annotation was generated for the fCotGob3.1 assembly using RNA-seq data generated from 4 tissues (brain, muscle, ovary, and spleen). The annotation for assembly fCotGob3.1 was released in Ensembl under database version 99.31 ( Hunt et al., 2018) (for fish clade annotation information see 2019-09: fish clade gene annotation). The resulting Ensembl annotation includes 60,811 transcripts assigned to 21,662 coding and 2,823 non-coding genes ( Channel bull blenny - Ensembl). RefSeq annotation is also available as NCBI Cottoperca gobio Annotation Release 100 ( Table 2).
Methods
Specimen acquisition and nucleic acid extractions
Both specimens used to generate the genome assembly were collected south of the Falkland Islands/Islas Malvinas in 2004 (Lat Long: -52° 40’, -59° 12’) during the ICEFISH 2004 Cruise (International Collaborative Expedition to collect and study Fish Indigenous to Sub-Antarctic Habitats; led by H. W. Detrich ( Detrich et al., 2012)) of the RVIB Nathaniel B. Palmer. Following euthanasia, fresh blood was collected from specimen fCotGob3, and spleen tissue (used for Hi-C) was collected from specimen fCotGob2 and was flash frozen in liquid nitrogen. Blood was processed immediately, whereas flash frozen spleen was preserved in the -80 freezer until processing. For RNA sequencing, tissue samples from two specimens were used (fCotGob2 - spleen, and fCotGob1 - brain, skeletal muscle, ovary). The additional tissues (fCotGob1) were preserved in RNALater and kept frozen until extraction. The tissues were sampled by T. Desvignes, H. W. Detrich, and J. H. Postlethwait from a specimen captured northwest of the Falkland Islands in 2018 by the Falkland Islands Fisheries Department ( Grass et al., 2018).
High molecular weight (HMW) DNA from fresh blood cells was prepared using an agarose plug extraction protocol ( Smith et al., 2010). Blood DNA was initially stabilised in agarose plugs and then shipped to Sanger Institute where the final steps of the extraction were performed using a BioNano Tissue extraction protocol. Quality control (QC) of HMW DNA was performed using the Femto Pulse instrument (Agilent). Total RNA was extracted from approximately 20–40 mg of tissue, from brain, skeletal muscle, ovary and spleen tissues using the RNeasy Qiagen extraction kit (Qiagen). QC was performed using Qubit HS RNA kit, and Agilent Bioanalyzer Nano chips. Only extracts with RIN value >8 were used for sequencing.
Sequencing
PacBio continuous long read (CLR) and 10X Genomics linked read sequencing libraries were constructed according to manufacturers’ instructions. Sequencing was performed by the Scientific Operations core at the Wellcome Sanger Institute on PacBio SEQUEL I and Illumina HiSeq X instruments. Hi-C data were generated using the Arima Hi-C kit v1 by Arima Genomics. BioNano data were generated on Saphyr (dual enzyme) at Bionano Genomics. RNA-seq was performed on HiSeq 4000 with 150bp insert paired end (PE) libraries.
Genome assembly
An initial PacBio assembly was made using Falcon-unzip ( Chin et al., 2016) without repeat-masking during overlap detection with Dazzler. The contigs from this assembly were first scaffolded by comparing them to a second wtdbg ( Ruan & Li, 2019) assembly using cross_genome, then they were scaffolded further using the 10X data with scaff10X, and then with BioNano two-enzyme hybrid scaffolding using Solve v3.2.1. The original PacBio data were then used to fill gaps with PBJelly ( English et al., 2012) and polish with Arrow. The resulting assembly was then polished again using the 10X Illumina data, by mapping with bwa mem ( Li, 2013), calling variants with freebayes ( Garrison & Marth, 2012), and correcting homozygous non-reference variants with bcftools consensus. Contiguity was increased further by filling gaps with the contigs from a second wtdgb assembly, which was made using PacBio reads corrected with Canu ( Koren et al., 2017). This assembly was re-polished with Arrow and freebayes, and retained haplotigs were identified with Purge Haplotigs ( Roach et al., 2018). Finally, the assembly was scaffolded to chromosomes using Arima Hi-C data with Salsa ( Ghurye et al., 2017). The scaffolded assembly was checked for contamination and manually improved using gEVAL ( Chow et al., 2016). The manual curation included steps such as correcting mis-joins, improving concordance with all available data types, and Hi-C 2D map visualized in Juicebox to produce complete chromosomal units ( Durand et al., 2016). Curation resulted in 9 manual breaks, 114 manual joins and the removal of 102 regions representing false duplications, decreasing the scaffold count by 39% to 322 and increasing the scaffold N50 by 68% to 25.2 Mb. The chromosomal-level scaffolds were named based on conserved synteny to the medaka assembly ( Oryzias latipes, Assembly accession GCA_002234675.1). The genome was further analysed within the BlobToolKit environment ( Challis et al., 2020). Software tools and versions used for assembly are listed in Table 3.
Table 3. Software tools used for genome assembly.
| Software tool | Version | Source |
|---|---|---|
| Falcon-
unzip |
falcon-2018.03.12-
04.00 |
( Chin et al., 2016) |
| wtdbg | 1.1 | ( Ruan & Li, 2019) |
| cross_
genome |
2014-08-22 |
https://sourceforge.
net/projects/phusion2/files/ cross_genome/ |
| PBJelly | PBSuite_15.8.24 | ( English et al., 2012) |
| Canu | 1.6 | ( Koren et al., 2017) |
| Purge
Haplotigs |
v1 | ( Roach et al., 2018) |
| Juicebox | (
Durand
et al., 2016;
Robinson et al., 2018) |
|
| scaff10x | 1.0 |
https://github.com/wtsi-
hpag/Scaff10X |
| Solve | Solve3.2.2_
08222018 |
https://bionanogenomics.
com/downloads/bionano- solve/ |
| arrow | GenomicConsensus
2.2.2 |
https://github.com/
PacificBiosciences/ GenomicConsensus |
| Bwa-mem | 0.7.17-r1188 | ( Li, 2013) |
| freebayes | v1.1.0-3-g961e5f3 | ( Garrison & Marth, 2012) |
| bcftools
consensus |
1.7 |
http://samtools.github.
io/bcftools/bcftools.html |
Data availability
Underlying data
European Nucleotide Archive: Cottoperca gobio (channel bull blenny) genome assembly, fCotGob3.1. BioProject accession number PRJEB30272; https://identifiers.org/ena.embl:PRJEB30272.
The C. gobio genome sequencing is part of the Wellcome Sanger Institute’s Vertebrate Sequencing project, and of the Vertebrate Genomes Project (VGP) ordinal references programme ( Rhie et al., 2020). All raw data and the assembly have been deposited in the ENA. Raw data and assembly accession identifiers are reported in Table 1.
Reporting guidelines
Not applicable.
Consent
Not applicable.
Author contributions
RD, JHP, HWD, SAM, IB: designed the experiment. IB, MS, KO: generated data. HWD, TD, JHP: provided samples. SAM, IB, JW, ZN, RD: performed data analysis. JW, WC, KH, JT: performed data curation. VGP Consortium: provided guidance for methodology development. EAM, RD: supervised the work and provided funding. IB: wrote the manuscript. All authors reviewed and edited the final version of the manuscript.
Acknowledgements
We thank Arima Genomics for generating the Hi-C library, Bionano Genomics for generating Saphyr optical mapping data, Prof. Erich Jarvis for comments on the manuscript, and Richard Challis for help with BlobToolKit.
Funding Statement
This work was supported by the Wellcome Trust through core funding to the Wellcome Sanger Institute (206194). IB, SAM and RD were supported by Wellcome grant 207492. HWD was supported by National Science Foundation grants OPP-0132032 (ICEFISH 2004 Cruise) and PLR-1444167. This work was also supported by grants from Wellcome (104640, 092096) to EAM. Publication number 29 from the ICEFISH Cruise of 2004 (HWD, Chief Scientist, RVIB Nathaniel B. Palmer). This is contribution 406 from the Marine Science Center at Northeastern University. JHP, HWD, and TD were supported by the National Science Foundation grant OPP-1543383.
The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
[version 1; peer review: 2 approved]
Author information
The Vertebrate Genomes Project Consortium includes Farooq O. Al-Ajli, Iliana Bista, Dave Burt, William Chow, Karen Clark, Hiram Clawson, Joanna Collins, Andrew J. Crawford, Joana Damas, Federica Di Palma, Mark Diekhans, Richard Durbin, Olivier Fedrigo, Paul Flicek, Giulio Formenti, Arkarachai Fungtammasan, Erik Garrison, Jay Ghurye, M. Thomas P. Gilbert, Jennifer Marshall Graves, Dengfeng Guan, Bettina Haase, Leanne Haggerty, Brett T. Hannigan, Robert S. Harris, Alex Hastie, David Haussler, Jinna Hoffman, Kevin Howe, Kerstin Howe, Erich D. Jarvis, Warren E. Johnson, Juwan Kim, Heebal Kim, Sarah B. Kingan, Byung June Ko, Klaus-Peter Koepfli, Sergey Koren, Jonas Korlach, Zev Kronenberg, Woori Kwak, Tanya M. Lama, Chul Lee, Joyce Lee, Harris Lewin, Kateryna D. Makova, Tomas Margues-Bonet, Fergal Martin, Patrick Masterson, Shane A. McCarthy, Paul Medvedev, Claudio V. Mello, Axel Meyer, Mark Mooney, Jacquelyn Mountcastle, Robert W. Murphy, Eugene W. Myers, Luis Nassar, Gavin J.P. Naylor, Zemin Ning, Stephen J. O’Brien, Sadye Paez, Benedict Paten, Sarah Pelan, Trevor Pesout, Adam M. Phillippy, Martin Pippel, Damon-Lee Pointon, Arang Rhie, Oliver A. Ryder, Simona Secomandi, Siddarth Selvaraj, Beth Shapiro, Maria Simbirsky, Ying Sims, Michelle Smith, Ivan Sovic, Emma C. Teeling, Constantina Theofanopoulou, Francoise Thibaud-Nissen, James Torrance, Alan Tracey, Marcela Uliano-Silva, Byrappa Venkatesh, Sonja C. Vernes, Brian P. Walenz, Tandy Warnow, Wesley C. Warren, Sylke Winkler, Jonathan Wood and Guojie Zhang.
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