Chromosome-Level Genome Assembly of Acanthogobius ommaturus Provides Insights Into Evolution and Lipid Metabolism

Acanthogobius ommaturus is a large, fast-growing annual fish widely distributed in coastal and estuarine areas. The adults will die after breeding, and its life cycle is only 1 year. The first chromosome-level genome assembly of A. ommaturus was obtained by PacBio and Hi-C sequencing in this study. The final genome assembly after Hi-C correction was 921.49 Mb, with contig N50 and scaffold N50 values of 15.70 Mb and 40.99 Mb, respectively. The assembled sequences were anchored to 22 chromosomes by using Hi-C data. A total of 18,752 protein-coding genes were predicted, 97.90% of which were successfully annotated. Benchmarking Universal Single-Copy Orthologs (BUSCO) assessment results for genome and gene annotations were 93.6% and 84.6%, respectively. A. ommaturus is phylogenetically closely related to Periophthalmodon magnuspinnatus and Boleophthalmus pectinirostris, diverging approximately 31.9 MYA with the two goby species. The A. ommaturus genome displayed 597 expanded and 3,094 contracted gene families compared with the common ancestor. A total of 1,155 positive selected genes (PSGs) (p < 0.05) were identified. Based on comparative genomic analyses, we obtained several expanded genes such as acsbg2, lrp1, lrp6, and znf638 involved in lipid metabolism. A total of twenty candidate genes were identified under positive selection, which associated with lifespan including ercc6, igf1, polg, and tert. Interspecific collinearity analysis showed a high genomic synteny between A. ommaturus and P. magnuspinnatus. The effective population size of A. ommaturus decreased drastically during 200–100 Ka because of Guxiang ice age and then increased gradually following warm periods. This study provides pivotal genetic resources for in-depth biological and evolutionary studies, and underlies the molecular basis for lipid metabolism.

[1]  Chenhong Li,et al.  A high-resolution genome of an euryhaline and eurythermal rhinogoby (Rhinogobius similis Gill 1895) , 2021, G3.

[2]  Fangrui Lou,et al.  Characterization and analysis of transcriptome complexity using SMRT-Seq combined with RNA-Seq for a better understanding of Acanthogobius ommaturus in response to temperature stress. , 2021, International journal of biological macromolecules.

[3]  Felipe A. Simão,et al.  BUSCO Update: Novel and Streamlined Workflows along with Broader and Deeper Phylogenetic Coverage for Scoring of Eukaryotic, Prokaryotic, and Viral Genomes , 2021, Molecular biology and evolution.

[4]  R. Blažek,et al.  Short‐lived fishes: Annual and multivoltine strategies , 2021 .

[5]  Meili Chen,et al.  Whole-genome sequencing reveals sex determination and liver high-fat storage mechanisms of yellowstripe goby (Mugilogobius chulae) , 2021, Communications biology.

[6]  Thomas M. Keane,et al.  Twelve years of SAMtools and BCFtools , 2020, GigaScience.

[7]  Fangrui Lou,et al.  Genomic characteristics and profile of microsatellite primers for Acanthogobius ommaturus by genome survey sequencing , 2020, Bioscience reports.

[8]  Manhong Liu,et al.  Chromosome‐level genome assembly of burbot (Lota lota) provides insights into the evolutionary adaptations in freshwater , 2020, Molecular ecology resources.

[9]  Jinmin Lian,et al.  Chromosome‐level genome assembly for the largemouth bass Micropterus salmoides provides insights into adaptation to fresh and brackish water , 2020, Molecular ecology resources.

[10]  Fangrui Lou,et al.  Gill Transcriptome Sequencing and De Novo Annotation of Acanthogobius ommaturus in Response to Salinity Stress , 2020, Genes.

[11]  Jiang Hu,et al.  NextPolish: a fast and efficient genome polishing tool for long-read assembly , 2019, Bioinform..

[12]  Xingtan Zhang,et al.  Assembly of allele-aware, chromosomal-scale autopolyploid genomes based on Hi-C data , 2019, Nature Plants.

[13]  Jiang Hu,et al.  De novo assembly of a chromosome‐level reference genome of red‐spotted grouper (Epinephelus akaara) using nanopore sequencing and Hi‐C , 2019, Molecular ecology resources.

[14]  L. Maltchik,et al.  Age-associated liver alterations in wild populations of Austrolebias minuano, a short-lived Neotropical annual killifish , 2019, Biogerontology.

[15]  V. Bohr,et al.  Cockayne syndrome group B deficiency reduces H3K9me3 chromatin remodeler SETDB1 and exacerbates cellular aging. , 2019, Nucleic acids research.

[16]  Songlin Chen,et al.  A chromosome‐level genome assembly of the giant grouper (Epinephelus lanceolatus) provides insights into its innate immunity and rapid growth , 2019, Molecular ecology resources.

[17]  Chao Bian,et al.  Divergence, evolution and adaptation in ray-finned fish genomes , 2019, Science China Life Sciences.

[18]  Jun Li,et al.  Genome sequence of the barred knifejaw Oplegnathus fasciatus (Temminck & Schlegel, 1844): the first chromosome-level draft genome in the family Oplegnathidae , 2019, GigaScience.

[19]  L. Castro,et al.  Expansion, retention and loss in the Acyl-CoA Synthetase “Bubblegum” (Acsbg) gene family in vertebrate history , 2018, bioRxiv.

[20]  O. Palluel,et al.  Liver histopathology and biochemical biomarkers in Gobius niger and Zosterisessor ophiocephalus from polluted and non-polluted Tunisian lagoons (Southern Mediterranean Sea). , 2018, Marine pollution bulletin.

[21]  Byrappa Venkatesh,et al.  The Divergent Genomes of Teleosts. , 2018, Annual review of animal biosciences.

[22]  Yury I. Miller,et al.  Modeling hypercholesterolemia and vascular lipid accumulation in LDL receptor mutant zebrafish[S] , 2017, Journal of Lipid Research.

[23]  Sudhir Kumar,et al.  TimeTree: A Resource for Timelines, Timetrees, and Divergence Times. , 2017, Molecular biology and evolution.

[24]  V. Bohr,et al.  Cockayne syndrome: Clinical features, model systems and pathways , 2017, Ageing Research Reviews.

[25]  A. Meyer,et al.  The seahorse genome and the evolution of its specialized morphology , 2016, Nature.

[26]  R. Blažek,et al.  Seasonal dynamics in community structure, abundance, body size and sex ratio in two species of Neotropical annual fishes. , 2016, Journal of fish biology.

[27]  J. Franco,et al.  Multi-organ histopathology in gobies for estuarine environmental risk assessment: A case study in the Ibaizabal estuary (SE Bay of Biscay) , 2016 .

[28]  Patricia P. Chan,et al.  tRNAscan-SE On-line: integrating search and context for analysis of transfer RNA genes , 2016, Nucleic Acids Res..

[29]  David Haussler,et al.  Long-read sequence assembly of the gorilla genome , 2016, Science.

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

[31]  Bronwen L. Aken,et al.  The spotted gar genome illuminates vertebrate evolution and facilitates human-to-teleost comparisons , 2016, Nature Genetics.

[32]  N. Berois,et al.  Annual Fishes : Life History Strategy, Diversity, and Evolution , 2015 .

[33]  Haibao Tang,et al.  jcvi: JCVI utility libraries , 2015 .

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

[35]  Param Priya Singh,et al.  A Platform for Rapid Exploration of Aging and Diseases in a Naturally Short-Lived Vertebrate , 2015, Cell.

[36]  Neva C. Durand,et al.  A 3D Map of the Human Genome at Kilobase Resolution Reveals Principles of Chromatin Looping , 2014, Cell.

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

[38]  R. Mahley,et al.  Apolipoprotein E: Structure and function in lipid metabolism, neurobiology, and Alzheimer's diseases , 2014, Neurobiology of Disease.

[39]  F. W. Keppeler,et al.  Abundance variations and life history traits of two sympatric species of Neotropical annual fish (Cyprinodontiformes: Rivulidae) in temporary ponds of southern Brazil , 2014 .

[40]  Alexandros Stamatakis,et al.  RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies , 2014, Bioinform..

[41]  Ziheng Yang,et al.  PAMLX: a graphical user interface for PAML. , 2013, Molecular biology and evolution.

[42]  Sean R. Eddy,et al.  Infernal 1.1: 100-fold faster RNA homology searches , 2013, Bioinform..

[43]  L. Partridge,et al.  The Hallmarks of Aging , 2013, Cell.

[44]  Cole Trapnell,et al.  TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions , 2013, Genome Biology.

[45]  Anton J. Enright,et al.  The zebrafish reference genome sequence and its relationship to the human genome , 2013, Nature.

[46]  S. Salzberg,et al.  TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions , 2013, Genome Biology.

[47]  S. Verhulst,et al.  Telomere length behaves as biomarker of somatic redundancy rather than biological age , 2013, Aging cell.

[48]  A. Zhavoronkov,et al.  The role of DNA damage and repair in aging through the prism of Koch-like criteria , 2013, Ageing Research Reviews.

[49]  G. Go,et al.  Low-Density Lipoprotein Receptor (LDLR) Family Orchestrates Cholesterol Homeostasis , 2012, The Yale journal of biology and medicine.

[50]  James R. Knight,et al.  The genome sequence of Atlantic cod reveals a unique immune system , 2011, Nature.

[51]  P. Chakrabarty The Biology of Gobies , 2011, Copeia.

[52]  R. Durbin,et al.  Inference of Human Population History From Whole Genome Sequence of A Single Individual , 2011, Nature.

[53]  A. Erol Deciphering the intricate regulatory mechanisms for the cellular choice between cell repair, apoptosis or senescence in response to damaging signals. , 2011, Cellular signalling.

[54]  L. Hugendubler,et al.  Regulation of Adipocyte Differentiation by the Zinc Finger Protein ZNF638 , 2011, The Journal of Biological Chemistry.

[55]  Carl Kingsford,et al.  A fast, lock-free approach for efficient parallel counting of occurrences of k-mers , 2011, Bioinform..

[56]  Qun Liu,et al.  Stock discrimination of spottedtail goby (Synechogobius ommaturus) in the Yellow Sea by analysis of otolith shape , 2011 .

[57]  Brian K. Kennedy,et al.  Progeria syndromes and ageing: what is the connection? , 2010, Nature Reviews Molecular Cell Biology.

[58]  M. Armanios Syndromes of telomere shortening. , 2009, Annual review of genomics and human genetics.

[59]  P. Rosenberg,et al.  Cancer in dyskeratosis congenita. , 2009, Blood.

[60]  Gonçalo R. Abecasis,et al.  The Sequence Alignment/Map format and SAMtools , 2009, Bioinform..

[61]  Claude-Alain H. Roten,et al.  Fast and accurate short read alignment with Burrows–Wheeler transform , 2009, Bioinform..

[62]  Matthias Platzer,et al.  Telomeres shorten while Tert expression increases during ageing of the short-lived fish Nothobranchius furzeri , 2009, Mechanisms of Ageing and Development.

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

[64]  Jonathan E. Allen,et al.  Automated eukaryotic gene structure annotation using EVidenceModeler and the Program to Assemble Spliced Alignments , 2007, Genome Biology.

[65]  D. Maiguel,et al.  Evidence for 26 distinct acyl-coenzyme A synthetase genes in the human genomes⃞s⃞ The online version of this article (available at http://www.jlr.org) contains supplementary data in the form of 3 Tables. Published, JLR Papers in Press, August 30, 2007. , 2007, Journal of Lipid Research.

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

[67]  D. Mickelson,et al.  Cosmogenic 10Be dating of Guxiang and Baiyu Glaciations , 2007 .

[68]  Keith Bradnam,et al.  CEGMA: a pipeline to accurately annotate core genes in eukaryotic genomes , 2007, Bioinform..

[69]  J. Hoeijmakers,et al.  Impaired Genome Maintenance Suppresses the Growth Hormone–Insulin-Like Growth Factor 1 Axis in Mice with Cockayne Syndrome , 2006, PLoS biology.

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

[71]  Jeffery P. Demuth,et al.  CAFE: a computational tool for the study of gene family evolution , 2006, Bioinform..

[72]  P. Watkins,et al.  The Second Member of the Human and Murine “Bubblegum” Family Is a Testis- and Brainstem-specific Acyl-CoA Synthetase* , 2006, Journal of Biological Chemistry.

[73]  João Pedro de Magalhães,et al.  HAGR: the Human Ageing Genomic Resources , 2004, Nucleic Acids Res..

[74]  Steven Salzberg,et al.  TigrScan and GlimmerHMM: two open source ab initio eukaryotic gene-finders , 2004, Bioinform..

[75]  A. Inoue,et al.  Comparative Histological Study of Teleost Livers in Relation to Phylogeny , 2004, Zoological science.

[76]  Thomas L. Madden,et al.  BLAST: at the core of a powerful and diverse set of sequence analysis tools , 2004, Nucleic Acids Res..

[77]  Robert C. Edgar,et al.  MUSCLE: multiple sequence alignment with high accuracy and high throughput. , 2004, Nucleic acids research.

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

[79]  V. Bohr,et al.  Cockayne syndrome group B cellular and biochemical functions. , 2003, American journal of human genetics.

[80]  C. Stoeckert,et al.  OrthoMCL: identification of ortholog groups for eukaryotic genomes. , 2003, Genome research.

[81]  D. Tocher Metabolism and Functions of Lipids and Fatty Acids in Teleost Fish , 2003 .

[82]  Michael J. Sanderson,et al.  R8s: Inferring Absolute Rates of Molecular Evolution, Divergence times in the Absence of a Molecular Clock , 2003, Bioinform..

[83]  Paramvir S. Dehal,et al.  Whole-Genome Shotgun Assembly and Analysis of the Genome of Fugu rubripes , 2002, Science.

[84]  R. Guigó,et al.  Using geneid to Identify Genes , 2002, Current protocols in bioinformatics.

[85]  T. M. Lewin,et al.  Do long-chain acyl-CoA synthetases regulate fatty acid entry into synthetic versus degradative pathways? , 2002, The Journal of nutrition.

[86]  Bergé,et al.  Mitochondrial and peroxisomal β-oxidation capacities in various tissues from Atlantic salmon Salmo salar. , 2000 .

[87]  Wei Qian,et al.  Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. , 2000, Molecular biology and evolution.

[88]  A. Meyer,et al.  Gene and genome duplications in vertebrates: the one-to-four (-to-eight in fish) rule and the evolution of novel gene functions. , 1999, Current opinion in cell biology.

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

[90]  P. Watkins Fatty acid activation. , 1997, Progress in lipid research.

[91]  S. Almatar,et al.  Seasonal Changes in the Lipid Composition of Herring (Clupea Harengus) in Relation to Gonad Maturation , 1989, Journal of the Marine Biological Association of the United Kingdom.

[92]  M. Brown,et al.  A receptor-mediated pathway for cholesterol homeostasis. , 1986, Science.

[93]  J. Sargent,et al.  Changes in the content and fatty acid composition of lipid in an isolated population of the capelin Mallotus villosus during sexual maturation and spawning , 1984 .

[94]  Chon-Kit Kenneth Chan,et al.  Analysis of RNA-Seq Data Using TopHat and Cufflinks. , 2016, Methods in molecular biology.

[95]  Huang We Analysis and Evaluation of Nutritional Components in Muscle of Cultured Synechogobius ommaturus , 2014 .

[96]  R. DePinho,et al.  Telomeres and telomerase in cancer. , 2010, Carcinogenesis.

[97]  David B. Wilson,et al.  Dyskeratosis congenita , 2010, FEBS letters.

[98]  A. Wolffe,et al.  PPARγ knockdown by engineered transcription factors: exogenous PPARγ2 but not PPARγ1 reactivates adipogenesis , 2002 .

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

[100]  Shun Guoyin,et al.  Ovarian Maturation and Spawning of Synechogobius ommaturus (Richardson) , 1996 .

[101]  J. Sargent,et al.  Fatty acid catabolism in the capelin, Mallotus villosus (Müller), during sexual maturation , 1984 .