A First Insight into the Genome of the Filter-Feeder Mussel Mytilus galloprovincialis

Mussels belong to the phylum Mollusca, one of the largest and most diverse taxa in the animal kingdom. Despite their importance in aquaculture and in biology in general, genomic resources from mussels are still scarce. To broaden and increase the genomic knowledge in this family, we carried out a whole-genome sequencing study of the cosmopolitan Mediterranean mussel (Mytilus galloprovincialis). We sequenced its genome (32X depth of coverage) on the Illumina platform using three pair-end libraries with different insert sizes. The large number of contigs obtained pointed out a highly complex genome of 1.6 Gb where repeated elements seem to be widespread (~30% of the genome), a feature that is also shared with other marine molluscs. Notwithstanding the limitations of our genome sequencing, we were able to reconstruct two mitochondrial genomes and predict 10,891 putative genes. A comparative analysis with other molluscs revealed a gene enrichment of gene ontology categories related to multixenobiotic resistance, glutamate biosynthetic process, and the maintenance of ciliary structures.

[1]  Tyler A. Elliott,et al.  What's in a genome? The C-value enigma and the evolution of eukaryotic genome content , 2015, Philosophical Transactions of the Royal Society B: Biological Sciences.

[2]  R. Tremblay,et al.  Ontogeny of bivalve immunity: assessing the potential of next-generation sequencing techniques , 2015 .

[3]  E. Verspoor,et al.  Patterns of natural selection acting on the mitochondrial genome of a locally adapted fish species , 2015, Genetics Selection Evolution.

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

[5]  Tyler A. Elliott,et al.  Do larger genomes contain more diverse transposable elements? , 2015, BMC Evolutionary Biology.

[6]  Jianzhi Zhang,et al.  Yeast mutation accumulation experiment supports elevated mutation rates at highly transcribed sites , 2014, Proceedings of the National Academy of Sciences.

[7]  L. Duret,et al.  Comparative population genomics in animals uncovers the determinants of genetic diversity , 2014, Nature.

[8]  A. Burzyński,et al.  Mitogenomics of recombinant mitochondrial genomes of Baltic Sea Mytilus mussels , 2014, Molecular Genetics and Genomics.

[9]  I. Bošnjak,et al.  Multixenobiotic Resistance Mechanism in Gills of Reared vs. Wild Mediterranean Mussel Mytilus galloprovincialis (Lamarck, 1819) , 2014, Water, Air, & Soil Pollution.

[10]  Hans Ellegren,et al.  Patterns of sequencing coverage bias revealed by ultra-deep sequencing of vertebrate mitochondria , 2014, BMC Genomics.

[11]  Shixia Xu,et al.  Adaptive Evolution of Mitochondrial Energy Metabolism Genes Associated with Increased Energy Demand in Flying Insects , 2014, PloS one.

[12]  H. Hummel,et al.  Glacial history of the European marine mussels Mytilus, inferred from distribution of mitochondrial DNA lineages , 2014, Heredity.

[13]  Huajun Zheng,et al.  Insights into Hepatopancreatic Functions for Nutrition Metabolism and Ovarian Development in the Crab Portunus trituberculatus: Gene Discovery in the Comparative Transcriptome of Different Hepatopancreas Stages , 2014, PloS one.

[14]  Derrick E. Wood,et al.  Kraken: ultrafast metagenomic sequence classification using exact alignments , 2014, Genome Biology.

[15]  Shijie Zhang,et al.  High genome heterozygosity and endemic genetic recombination in the wheat stripe rust fungus , 2013, Nature Communications.

[16]  S. Yum,et al.  Expressions of oxidative stress-related genes and antioxidant enzyme activities in Mytilus galloprovincialis (Bivalvia, Mollusca) exposed to hypoxia , 2013, Zoological Studies.

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

[18]  S. Searle,et al.  The duck genome and transcriptome provide insight into an avian influenza virus reservoir species , 2013, Nature Genetics.

[19]  L. Bachmann,et al.  Reconstructing mitochondrial genomes directly from genomic next-generation sequencing reads—a baiting and iterative mapping approach , 2013, Nucleic acids research.

[20]  Pamela M. Brannock,et al.  Ubiquitous heteroplasmy in Mytilus spp. resulting from disruption in doubly uniparental inheritance regulation , 2013 .

[21]  H. Nagasawa,et al.  Mollusk shell structures and their formation mechanism1 , 2013 .

[22]  D. Casane,et al.  Accommodating the load , 2013, Mobile genetic elements.

[23]  J. Ausió,et al.  The CHROMEVALOA Database: A Resource for the Evaluation of Okadaic Acid Contamination in the Marine Environment Based on the Chromatin-Associated Transcriptome of the Mussel Mytilus galloprovincialis , 2013, Marine drugs.

[24]  Inanç Birol,et al.  Assemblathon 2: evaluating de novo methods of genome assembly in three vertebrate species , 2013, GigaScience.

[25]  Nicholas H. Putnam,et al.  Insights into bilaterian evolution from three spiralian genomes , 2012, Nature.

[26]  P. Kamermans,et al.  A glimpse of the mollusc industry in Europe , 2013 .

[27]  Damon Lisch,et al.  How important are transposons for plant evolution? , 2012, Nature Reviews Genetics.

[28]  Bjarne Knudsen,et al.  First draft genome sequence of the Japanese eel, Anguilla japonica. , 2012, Gene.

[29]  J. Merilä,et al.  Whole mitochondrial genome scan for population structure and selection in the Atlantic herring , 2012, BMC Evolutionary Biology.

[30]  Jianzhi Zhang,et al.  Genomic evidence for elevated mutation rates in highly expressed genes , 2012, EMBO reports.

[31]  Christoph Held,et al.  Exploring Pandora's Box: Potential and Pitfalls of Low Coverage Genome Surveys for Evolutionary Biology , 2012, PloS one.

[32]  N. Fedoroff.  Transposable Elements, Epigenetics, and Genome Evolution , 2012 .

[33]  B. Chénais,et al.  The impact of transposable elements on eukaryotic genomes: from genome size increase to genetic adaptation to stressful environments. , 2012, Gene.

[34]  Qiang Wang,et al.  The oyster genome reveals stress adaptation and complexity of shell formation , 2012, Nature.

[35]  Shane S. Sturrock,et al.  Geneious Basic: An integrated and extendable desktop software platform for the organization and analysis of sequence data , 2012, Bioinform..

[36]  Steven L Salzberg,et al.  Fast gapped-read alignment with Bowtie 2 , 2012, Nature Methods.

[37]  Hideo Aoki,et al.  Draft Genome of the Pearl Oyster Pinctada fucata: A Platform for Understanding Bivalve Biology , 2012, DNA research : an international journal for rapid publication of reports on genes and genomes.

[38]  Robert D. Finn,et al.  InterPro in 2011: new developments in the family and domain prediction database , 2011, Nucleic acids research.

[39]  Mark Yandell,et al.  MAKER2: an annotation pipeline and genome-database management tool for second-generation genome projects , 2011, BMC Bioinformatics.

[40]  Jesse M. Platt,et al.  Hypoxia promotes isocitrate dehydrogenase-dependent carboxylation of α-ketoglutarate to citrate to support cell growth and viability , 2011, Proceedings of the National Academy of Sciences.

[41]  A. Pallavicini,et al.  Massively Parallel Amplicon Sequencing Reveals Isotype-Specific Variability of Antimicrobial Peptide Transcripts in Mytilus galloprovincialis , 2011, PloS one.

[42]  John F. Dishinger,et al.  Kinesin motors and primary cilia. , 2011, Biochemical Society transactions.

[43]  J. Sese,et al.  Genome structure analysis of molluscs revealed whole genome duplication and lineage specific repeat variation. , 2011, Gene.

[44]  J. Rotchell,et al.  Identification of Reproduction-Specific Genes Associated with Maturation and Estrogen Exposure in a Marine Bivalve Mytilus edulis , 2011, PloS one.

[45]  David M. A. Martin,et al.  Genome sequence and analysis of the tuber crop potato , 2011, Nature.

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

[47]  A. Figueras,et al.  New Insights into the Apoptotic Process in Mollusks: Characterization of Caspase Genes in Mytilus galloprovincialis , 2011, PloS one.

[48]  P. Wade,et al.  Positive selection on the killer whale mitogenome , 2011, Biology Letters.

[49]  G. Lanfranchi,et al.  Insights into the innate immunity of the Mediterranean mussel Mytilus galloprovincialis , 2011, BMC Genomics.

[50]  E. Lerat.  Identifying repeats and transposable elements in sequenced genomes: how to find your way through the dense forest of programs , 2010, Heredity.

[51]  Richard G Melvin,et al.  Linking the mitochondrial genotype to the organismal phenotype , 2010, Molecular ecology.

[52]  Jack A. Gilbert,et al.  Pyrosequencing of Mytilus galloprovincialis cDNAs: Tissue-Specific Expression Patterns , 2010, PloS one.

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

[54]  Taichi E. Takasuka,et al.  Are nucleosome positions in vivo primarily determined by histone–DNA sequence preferences? , 2009, Nucleic acids research.

[55]  Asan,et al.  The genome of the cucumber, Cucumis sativus L. , 2009, Nature Genetics.

[56]  N. Hirokawa,et al.  Kinesin superfamily motor proteins and intracellular transport , 2009, Nature Reviews Molecular Cell Biology.

[57]  E. Kenchington,et al.  Paternal mtDNA and Maleness Are Co-Inherited but Not Causally Linked in Mytilid Mussels , 2009, PloS one.

[58]  David A. Rasmussen,et al.  What can you do with 0.1× genome coverage? A case study based on a genome survey of the scuttle fly Megaselia scalaris (Phoridae) , 2009, BMC Genomics.

[59]  D. Lallias,et al.  Characterization of Ten Microsatellite Loci in the Blue Mussel Mytilus edulis , 2009 .

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

[61]  F. Leboulenger,et al.  Tidal height influences the levels of enzymatic antioxidant defences in Mytilus edulis. , 2009, Marine environmental research.

[62]  Keith Bradnam,et al.  Assessing the gene space in draft genomes , 2008, Nucleic acids research.

[63]  G. Lanfranchi,et al.  MytiBase: a knowledgebase of mussel (M. galloprovincialis) transcribed sequences , 2009, BMC Genomics.

[64]  Francois Sabot,et al.  Low-pass shotgun sequencing of the barley genome facilitates rapid identification of genes, conserved non-coding sequences and novel repeats , 2008, BMC Genomics.

[65]  A. Pallavicini,et al.  Study of Diseases and the Immune System of Bivalves Using Molecular Biology and Genomics , 2008 .

[66]  B. Watermann,et al.  Pathology and mass mortality of Pacific oysters, Crassostrea gigas (Thunberg), in 2005 at the East Frisian coast, Germany. , 2008, Journal of Fish Diseases.

[67]  Hiroaki Takagi,et al.  Functional Analysis of Spontaneous Cell Movement under Different Physiological Conditions , 2008, PloS one.

[68]  Laura A. MacManus-Spencer,et al.  Efflux transporters: newly appreciated roles in protection against pollutants. , 2008, Environmental science & technology.

[69]  D. Epel,et al.  ABCB- and ABCC-type transporters confer multixenobiotic resistance and form an environment-tissue barrier in bivalve gills. , 2008, American journal of physiology. Regulatory, integrative and comparative physiology.

[70]  Steve Widdicombe,et al.  Effects of ocean acidification on the immune response of the blue mussel Mytilus edulis , 2008 .

[71]  A. P. Diz,et al.  Regional patterns of microsatellite variation in Mytilus galloprovincialis from the Iberian Peninsula , 2008 .

[72]  C. Feschotte,et al.  DNA transposons and the evolution of eukaryotic genomes. , 2007, Annual review of genetics.

[73]  F. Roberto,et al.  Understanding Marine Mussel Adhesion , 2007, Marine Biotechnology.

[74]  J. Jurka,et al.  Repetitive sequences in complex genomes: structure and evolution. , 2007, Annual review of genomics and human genetics.

[75]  P. Blier,et al.  The unusual system of doubly uniparental inheritance of mtDNA: isn't one enough? , 2007, Trends in genetics : TIG.

[76]  Antonio Figueras Huerta.  Biología y cultivo del mejillón (Mytilus galloprovincialis) en Galicia , 2007 .

[77]  E. Zouros,et al.  Nucleotide Content Gradients in Maternally and Paternally Inherited Mitochondrial Genomes of the Mussel Mytilus , 2007, Journal of Molecular Evolution.

[78]  Juan Miguel García-Gómez,et al.  BIOINFORMATICS APPLICATIONS NOTE Sequence analysis Manipulation of FASTQ data with Galaxy , 2005 .

[79]  T. Gregory.  Synergy between sequence and size in Large-scale genomics , 2005, Nature Reviews Genetics.

[80]  P. Venier,et al.  Characterization of mussel gill cells in vivo and in vitro , 2005, Cell and Tissue Research.

[81]  S. Cole,et al.  Multidrug resistance proteins: role of P-glycoprotein, MRP1, MRP2, and BCRP (ABCG2) in tissue defense. , 2005, Toxicology and applied pharmacology.

[82]  N. Moschonas,et al.  The complete maternal and paternal mitochondrial genomes of the Mediterranean mussel Mytilus galloprovincialis: implications for the doubly uniparental inheritance mode of mtDNA. , 2005, Molecular biology and evolution.

[83]  J. Pouysségur,et al.  When hypoxia signalling meets the ubiquitin-proteasomal pathway, new targets for cancer therapy. , 2005, Critical reviews in oncology/hematology.

[84]  D. Wildman,et al.  Accelerated evolution of the electron transport chain in anthropoid primates. , 2004, Trends in genetics : TIG.

[85]  Ian Korf,et al.  Gene finding in novel genomes , 2004, BMC Bioinformatics.

[86]  S. Salzberg,et al.  Versatile and open software for comparing large genomes , 2004, Genome Biology.

[87]  Alberto Pallavicini,et al.  Towards a catalogue of genes transcribed in multiple tissues of Mytilus galloprovincialis. , 2003, Gene.

[88]  B. Miflin,et al.  Glutamate synthase and the synthesis of glutamate in plants , 2003 .

[89]  Wu-chun Feng,et al.  The design, implementation, and evaluation of mpiBLAST , 2003 .

[90]  S. Lewis,et al.  The generic genome browser: a building block for a model organism system database. , 2002, Genome research.

[91]  P. David,et al.  ASSORTATIVE FERTILIZATION AND SELECTION AT LARVAL STAGE IN THE MUSSELS MYTILUS EDULIS AND M. GALLOPROVINCIALIS , 2002, Evolution; international journal of organic evolution.

[92]  E. Zouros,et al.  The exceptional mitochondrial DNA system of the mussel family Mytilidae. , 2000, Genes & genetic systems.

[93]  J. Himmelman,et al.  Reproduction and summer mortality of blue mussels Mytilus edulis in the Magdalen Islands, southern Gulf of St. Lawrence , 2000 .

[94]  S. Iida,et al.  Molecular characterization of the mutable flaked allele for flower variegation in the common morning glory. , 1998, The Plant journal : for cell and molecular biology.

[95]  P. Rawson,et al.  ASYMMETRIC INTROGRESSION OF MITOCHONDRIAL DNA AMONG EUROPEAN POPULATIONS OF BLUE MUSSELS (MYTILUS SPP.) , 1998, Evolution; international journal of organic evolution.

[96]  V. Corces,et al.  Penelope, a new family of transposable elements and its possible role in hybrid dysgenesis in Drosophila virilis. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[97]  P. Rawson,et al.  Evidence for intragenic recombination within a novel genetic marker that distinguishes mussels in the Mytilus edulis species complex , 1996, Heredity.

[98]  M. Torrado,et al.  Genome-size variation in bivalve molluscs determined by flow cytometry , 1996 .

[99]  D. Skibinski,et al.  Sex-limited mitochondrial DNA transmission in the marine mussel Mytilus edulis. , 1994, Genetics.

[100]  C. Saavedra,et al.  An unusual type of mitochondrial DNA inheritance in the blue mussel Mytilus. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[101]  T. Tan,et al.  Chromosomes and nuclear DNA contents of some species in Mytilidae , 1994 .

[102]  B. Kurelec.  The multixenobiotic resistance mechanism in aquatic organisms. , 2002, Critical reviews in toxicology.

[103]  E. Lozovskaya,et al.  A hybrid dysgenesis syndrome in Drosophila virilis. , 1990, Genetics.

[104]  E. Myers,et al.  Basic local alignment search tool. , 1990, Journal of molecular biology.

[105]  M. Monastirioti,et al.  hobo is responsible for the induction of hybrid dysgenesis by strains of Drosophila melanogaster bearing the male recombination factor 23.5MRF , 1987, Cell.

[106]  M. Cherry,et al.  Mytilus galloprovincialis Lmk. in Southern Africa , 1985 .

[107]  P. Gaffney,et al.  Genetic heterozygosity and growth rate in Mytilus edulis , 1984 .

[108]  C. Thiriot-Quiéveux,et al.  Les caryotypes de quelques espèces de bivalves et de gastéropodes marins , 1982 .

[109]  D. Skibinski,et al.  Electrophoretic investigation of systematic relationships in the marine mussels Modiolus modiolus L., Mytilus edulis L., and Mytilus galloprovincialis Lmk. (Mytilidae; Mollusca) , 1980 .

[110]  M. StanleyS.  Adaptive Themes in the Evolution of the Bivalvia (Mollusca) , 1975 .