Whole genome sequencing of the fast-swimming Southern bluefin tuna (Thunnus maccoyii)

The economically important Southern bluefin tuna (Thunnus maccoyii) is a world-famous fast-swimming fish, but its genomic information is limited. Here, we performed whole genome sequencing and assembled a draft genome for Southern bluefin tuna, aiming to generate useful genetic data for comparative functional prediction. The final genome assembly is 806.54 Mb, with scaffold and contig N50 values of 3.31 Mb and 67.38 kb, respectively. Genome completeness was evaluated to be 95.8%. The assembled genome contained 23,403 protein-coding genes and 236.1 Mb of repeat sequences (accounting for 29.27% of the entire assembly). Comparative genomics analyses of this fast-swimming tuna revealed that it had more than twice as many hemoglobin genes (18) as other relatively slow-moving fishes (such as seahorse, sunfish, and tongue sole). These hemoglobin genes are mainly localized in two big clusters (termed as “MNˮ and “LAˮ respectively), which is consistent with other reported fishes. However, Thr39 of beta-hemoglobin in the MN cluster, conserved in other fishes, was mutated as cysteine in tunas including the Southern bluefin tuna. Since hemoglobins are reported to transport oxygen efficiently for aerobic respiration, our genomic data suggest that both high copy numbers of hemoglobin genes and an adjusted function of the beta-hemoglobin may support the fast-swimming activity of tunas. In summary, we produced a primary genome assembly and predicted hemoglobin-related roles for the fast-swimming Southern bluefin tuna.

[1]  Yuan Yuan,et al.  The Genomes of Two Billfishes Provide Insights into the Evolution of Endothermy in Teleosts , 2021, Molecular biology and evolution.

[2]  Shunping He,et al.  Recent genome duplications facilitate the phenotypic diversity of Hb repertoire in the Cyprinidae , 2020, Science China Life Sciences.

[3]  B. Venkatesh,et al.  Oxygenation properties of hemoglobin and the evolutionary origins of isoform multiplicity in an amphibious air-breathing fish, the blue-spotted mudskipper (Boleophthalmus pectinirostris) , 2019, Journal of Experimental Biology.

[4]  K. Schneeberger,et al.  SyRI: finding genomic rearrangements and local sequence differences from whole-genome assemblies , 2019, Genome Biology.

[5]  N. Suzuki,et al.  Improvement of the Pacific bluefin tuna (Thunnus orientalis) reference genome and development of male-specific DNA markers , 2019, Scientific Reports.

[6]  Xingang Wang,et al.  RaGOO: fast and accurate reference-guided scaffolding of draft genomes , 2019, Genome Biology.

[7]  A. Kimoto,et al.  Spatial dynamics and mixing of bluefin tuna in the Atlantic Ocean and Mediterranean Sea revealed using next‐generation sequencing , 2018, Molecular ecology resources.

[8]  R. Brill,et al.  Sharing the water column: physiological mechanisms underlying species-specific habitat use in tunas , 2017, Reviews in Fish Biology and Fisheries.

[9]  Han Fang,et al.  GenomeScope: Fast reference-free genome profiling from short reads , 2016, bioRxiv.

[10]  Thomas K. F. Wong,et al.  ModelFinder: Fast Model Selection for Accurate Phylogenetic Estimates , 2017, Nature Methods.

[11]  R. Hanel,et al.  Genomic Differentiation and Demographic Histories of Atlantic and Indo-Pacific Yellowfin Tuna (Thunnus albacares) Populations , 2017, Genome biology and evolution.

[12]  J. F. Storz Gene Duplication and Evolutionary Innovations in Hemoglobin-Oxygen Transport. , 2016, Physiology.

[13]  Sudhir Kumar,et al.  MEGA7: Molecular Evolutionary Genetics Analysis Version 7.0 for Bigger Datasets. , 2016, Molecular biology and evolution.

[14]  Heng Li,et al.  Minimap and miniasm: fast mapping and de novo assembly for noisy long sequences , 2015, Bioinform..

[15]  Siu-Ming Yiu,et al.  Erratum: SOAPdenovo2: an empirically improved memory-efficient short-read de novo assembler , 2015, GigaScience.

[16]  O. Kohany,et al.  Repbase Update, a database of repetitive elements in eukaryotic genomes , 2015, Mobile DNA.

[17]  Bo Hu,et al.  GSDS 2.0: an upgraded gene feature visualization server , 2014, Bioinform..

[18]  A. von Haeseler,et al.  IQ-TREE: A Fast and Effective Stochastic Algorithm for Estimating Maximum-Likelihood Phylogenies , 2014, Molecular biology and evolution.

[19]  Alessandro Vullo,et al.  Ensembl 2015 , 2014, Nucleic Acids Res..

[20]  Ying Sun,et al.  Mudskipper genomes provide insights into the terrestrial adaptation of amphibious fishes , 2014, Nature Communications.

[21]  T. Burmester,et al.  The globin gene repertoire of lampreys: convergent evolution of hemoglobin and myoglobin in jawed and jawless vertebrates. , 2014, Molecular biology and evolution.

[22]  Tetsuya Hayashi,et al.  Efficient de novo assembly of highly heterozygous genomes from whole-genome shotgun short reads , 2014, Genome research.

[23]  Zhanjiang Liu,et al.  Channel catfish hemoglobin genes: identification, phylogenetic and syntenic analysis, and specific induction in response to heat stress. , 2014, Comparative biochemistry and physiology. Part D, Genomics & proteomics.

[24]  Guojie Zhang,et al.  Whole-genome sequence of a flatfish provides insights into ZW sex chromosome evolution and adaptation to a benthic lifestyle , 2014, Nature Genetics.

[25]  Jianying Yuan,et al.  Estimation of genomic characteristics by analyzing k-mer frequency in de novo genome projects , 2013, 1308.2012.

[26]  J. Hoyer,et al.  Hb Grove City [β38(C4)Thr→Ser, ACC>AGC; HBB: c.116C>G]: A New Low Oxygen Affinity β Chain Variant , 2013, Hemoglobin.

[27]  M. Hattori,et al.  Evolutionary changes of multiple visual pigment genes in the complete genome of Pacific bluefin tuna , 2013, Proceedings of the National Academy of Sciences.

[28]  F. Hoffmann,et al.  Gene duplication, genome duplication, and the functional diversification of vertebrate globins. , 2013, Molecular phylogenetics and evolution.

[29]  F. Hoffmann,et al.  Whole-Genome Duplication and the Functional Diversification of Teleost Fish Hemoglobins , 2012, Molecular biology and evolution.

[30]  R. Hardison Evolution of hemoglobin and its genes. , 2012, Cold Spring Harbor perspectives in medicine.

[31]  F. Hoffmann,et al.  Whole-genome duplications spurred the functional diversification of the globin gene superfamily in vertebrates. , 2012, Molecular biology and evolution.

[32]  E. Carlson,et al.  Human Biology and Health , 2009, The Quarterly Review of Biology.

[33]  Keith A. Boroevich,et al.  Genomic organization and evolution of the Atlantic salmon hemoglobin repertoire , 2010, BMC Genomics.

[34]  F. Hoffmann,et al.  Gene cooption and convergent evolution of oxygen transport hemoglobins in jawed and jawless vertebrates , 2010, Proceedings of the National Academy of Sciences.

[35]  Cole Trapnell,et al.  Role of Rodent Secondary Motor Cortex in Value-based Action Selection Nih Public Access Author Manuscript , 2006 .

[36]  O. Gascuel,et al.  New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. , 2010, Systematic biology.

[37]  Dawei Li,et al.  The sequence and de novo assembly of the giant panda genome , 2010, Nature.

[38]  György Abrusán,et al.  TEclass - a tool for automated classification of unknown eukaryotic transposable elements , 2009, Bioinform..

[39]  Lior Pachter,et al.  Sequence Analysis , 2020, Definitions.

[40]  Nansheng Chen,et al.  Using RepeatMasker to Identify Repetitive Elements in Genomic Sequences , 2009, Current protocols in bioinformatics.

[41]  Robert D. Finn,et al.  InterPro: the integrative protein signature database , 2008, Nucleic Acids Res..

[42]  G. Hays,et al.  The biology and ecology of the ocean sunfish Mola mola: a review of current knowledge and future research perspectives , 2009, Reviews in Fish Biology and Fisheries.

[43]  E. Birney,et al.  Pfam: the protein families database , 2013, Nucleic Acids Res..

[44]  R. Hardison Globin genes on the move , 2008, Journal of biology.

[45]  C. ozouF-cosTaz,et al.  Comparative and evolutionary genomics of globin genes in fish. , 2008, Methods in enzymology.

[46]  C. Verde,et al.  Inferring evolution of fish proteins: the globin case study. , 2008, Methods in enzymology.

[47]  Barbara A. Block,et al.  Temperature effects on metabolic rate of juvenile Pacific bluefin tuna Thunnus orientalis , 2007, Journal of Experimental Biology.

[48]  F. Hoffmann,et al.  The αD-Globin Gene Originated via Duplication of an Embryonic α-Like Globin Gene in the Ancestor of Tetrapod Vertebrates , 2007 .

[49]  H. A. Rutjes,et al.  Multiple strategies of Lake Victoria cichlids to cope with lifelong hypoxia include hemoglobin switching. , 2007, American journal of physiology. Regulatory, integrative and comparative physiology.

[50]  David W Mount,et al.  Using the Basic Local Alignment Search Tool (BLAST). , 2007, CSH protocols.

[51]  Zhao Xu,et al.  LTR_FINDER: an efficient tool for the prediction of full-length LTR retrotransposons , 2007, Nucleic Acids Res..

[52]  B. Block,et al.  Influence of Swimming Speed on Metabolic Rates of Juvenile Pacific Bluefin Tuna and Yellowfin Tuna , 2007, Physiological and Biochemical Zoology.

[53]  G. Weinstock,et al.  Creating a honey bee consensus gene set , 2007, Genome Biology.

[54]  C. Verde,et al.  The evolution of thermal adaptation in polar fish. , 2006, Gene.

[55]  Yongwei Wei,et al.  Characterization of the 5'-to-5'linked adult alpha- and beta-globin genes from three sciaenid fish species (Pseudosciaena crocea, Sciaenops ocellatus, Nibea miichthioides). , 2006, Comparative biochemistry and physiology. Part D, Genomics & proteomics.

[56]  C. Verde,et al.  Molecular evolution of haemoglobins of polar fishes , 2006 .

[57]  Burkhard Morgenstern,et al.  AUGUSTUS: ab initio prediction of alternative transcripts , 2006, Nucleic Acids Res..

[58]  J. Jurka,et al.  Repbase Update, a database of eukaryotic repetitive elements , 2005, Cytogenetic and Genome Research.

[59]  Sébastien Carrère,et al.  The ProDom database of protein domain families: more emphasis on 3D , 2004, Nucleic Acids Res..

[60]  Ewan Birney,et al.  Automated generation of heuristics for biological sequence comparison , 2005, BMC Bioinformatics.

[61]  K. Maruyama,et al.  Evolution of globin genes of the medaka Oryzias latipes (Euteleostei; Beloniformes; Oryziinae) , 2004, Mechanisms of Development.

[62]  R. Durbin,et al.  GeneWise and Genomewise. , 2004, Genome research.

[63]  G. Parkes Fishes of the Southern Ocean , 1992, Reviews in Fish Biology and Fisheries.

[64]  Peer Bork,et al.  SMART 4.0: towards genomic data integration , 2004, Nucleic Acids Res..

[65]  Maria Jesus Martin,et al.  The SWISS-PROT protein knowledgebase and its supplement TrEMBL in 2003 , 2003, Nucleic Acids Res..

[66]  Terri K. Attwood,et al.  The PRINTS Database: A Resource for Identification of Protein Families , 2002, Briefings Bioinform..

[67]  F. Jensen Hydrogen ion binding properties of tuna haemoglobins. , 2001, Comparative biochemistry and physiology. Part A, Molecular & integrative physiology.

[68]  Webb Miller,et al.  Comparative genome analysis delimits a chromosomal domain and identifies key regulatory elements in the α globin cluster , 2001 .

[69]  J. Stamler,et al.  Export by red blood cells of nitric oxide bioactivity , 2001, Nature.

[70]  Eric Beitz,et al.  TeXshade: shading and labeling of multiple sequence alignments using LaTeX2e , 2000, Bioinform..

[71]  Susumu Goto,et al.  KEGG: Kyoto Encyclopedia of Genes and Genomes , 2000, Nucleic Acids Res..

[72]  G. Benson,et al.  Tandem repeats finder: a program to analyze DNA sequences. , 1999, Nucleic acids research.

[73]  T. Aoki,et al.  Head-to-head linkage of carp α- and β-globin genes , 1997 .

[74]  S. Karlin,et al.  Prediction of complete gene structures in human genomic DNA. , 1997, Journal of molecular biology.

[75]  A. Brownlie,et al.  Characterization of Adult α- and β-Globin Genes in the Zebrafish , 1997 .

[76]  T. Aoki,et al.  Head-to-head linkage of carp alpha- and beta-globin genes. , 1997, Biochimica et biophysica acta.

[77]  S. R. Kerr,et al.  Effect of activity level on apparent heat increment in Atlantic cod, Gadus morhua , 1996 .

[78]  Y. Shimizu,et al.  Variations in I-V characteristics of oxide semiconductors induced by oxidizing gases , 1996 .

[79]  A. Cao,et al.  Hb Hinwil or β38(C4)THR→ASN: A new β Chain Variant Detected in a Swiss Family , 1996 .

[80]  H. Dewar,et al.  The aerobic capacity of tunas: Adaptation for multiple metabolic demands , 1996 .

[81]  Richard W. Brill,et al.  Selective advantages conferred by the high performance physiology of tunas, billfishes, and dolphin fish , 1996 .

[82]  Y. Wada,et al.  Site-directed mutagenesis in hemoglobin: functional and structural study of the intersubunit hydrogen bond of threonine-38(C3)alpha at the alpha 1-beta 2 interface in human hemoglobin. , 1993, Biochemistry.

[83]  Pingguo He,et al.  The muscle twitch and the maximum swimming speed of giant bluefin tuna, Thunnus thynnus L. , 1989 .

[84]  Y. Blouquit,et al.  Structural study of hemoglobin Hazebrouck, beta 38(C4)Thr----Pro. A new abnormal hemoglobin with instability and low oxygen affinity. , 1984, FEBS letters.

[85]  Richard Earl Dickerson,et al.  Hemoglobin : structure, function, evolution, and pathology , 1983 .

[86]  R. W. Blake,et al.  On seahorse locomotion , 1976, Journal of the Marine Biological Association of the United Kingdom.

[87]  Morris Goodman,et al.  Darwinian evolution in the genealogy of haemoglobin , 1975, Nature.

[88]  J. Magnuson COMPARATIVE STUDY OF ADAPTATIONS FOR CONTINUOUS SWIMMING AND HYDROSTATIC EQUILIBRIUM OF SCOMBROID AND XIPHOID FISHES , 1973 .

[89]  W. Hendrickson,et al.  Structure of lamprey haemoglobin. , 1971, Nature: New biology.

[90]  M. F. PERUTZ,et al.  Three Dimensional Fourier Synthesis of Horse Deoxyhaemoglobin at 2.8 Å Resolution , 1970, Nature.