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Published April 2013 | Supplemental Material + Published
Journal Article Open

Sequencing of the sea lamprey (Petromyzon marinus) genome provides insights into vertebrate evolution

Smith, Jeramiah J. ORCID icon
Sauka-Spengler, Tatjana ORCID icon
Jones, Matthew
Bronner, Marianne E. ORCID icon

Abstract

Lampreys are representatives of an ancient vertebrate lineage that diverged from our own ~500 million years ago. By virtue of this deeply shared ancestry, the sea lamprey (P. marinus) genome is uniquely poised to provide insight into the ancestry of vertebrate genomes and the underlying principles of vertebrate biology. Here, we present the first lamprey whole-genome sequence and assembly. We note challenges faced owing to its high content of repetitive elements and GC bases, as well as the absence of broad-scale sequence information from closely related species. Analyses of the assembly indicate that two whole-genome duplications likely occurred before the divergence of ancestral lamprey and gnathostome lineages. Moreover, the results help define key evolutionary events within vertebrate lineages, including the origin of myelin-associated proteins and the development of appendages. The lamprey genome provides an important resource for reconstructing vertebrate origins and the evolutionary events that have shaped the genomes of extant organisms.

Additional Information

© 2013 Nature Publishing Group. This work is licensed under a Creative Commons Attribution- NonCommercial-Share Alike 3.0 Unported License. To view a copy of this license, visit http://creativecommons.org/licenses/by-nc-sa/3.0/. Received 20 July 2012; accepted 31 January 2013; published online 24 February 2013. We thank the Genome Institute, Washington University School of Medicine, Production Sequencing group for all sample procurement and genome sequencing work, the Michigan State University Genomic Core for transcriptome sequencing and the US Geological Survey, Lake Huron Biological Station for providing lamprey samples for sequencing. We thank F. Antonacci and E.E. Eichler (University of Washington) for performing FISH and providing access to computational facilities, respectively. We thank M. Robinson for bioinformatic analysis of immune system–related genes and conversion of GFF files for BAC end mapping. A portion of this research was conducted at the Marine Biological Laboratory (Woods Hole, Massachusetts). We acknowledge the support of the Stowers Institute for Medical Research (SIMR) and technical support from the SIMR Molecular Biology Core, particularly K. Staehling, A. Perera and K. Delventhal for BAC screening and sequencing. We acknowledge the Center for High-Performance Computing at the University of Utah for the allocation of computational resources toward gene annotation. We recognize all the important work that could not be cited owing to space limitations. The lamprey genome project was funded by the National Human Genome Research Institute (U54HG003079 (R.K.W.)). Additional support was provided by grants from the US National Institutes of Health (R24GM83982 (W.L.)) and the Great Lakes Fisheries commission (W.L.). Partial funding was provided by several additional sources, including grants from the US National Institutes of Health (F32GM087919 and T32HG00035 (J.J.S.); DE017911 (M.E.B.); R03NS078519 (O.E.B.); R01HG004694 (M.D.Y.); GM079492, GM090049 and RR014085 (C.T.A.); and R37HD032443 (C.J.T.)), the National Science Foundation (MCB-0719558 (C.T.A.); IOS-0849569 (S.A.S.); IBN-0208138 (L. Holland); and IOS-1126998 (M.D.Y.)), the New Hampshire Agricultural Experiment Station (Scientific Contribution Number 2471 (S.A.S.)), the Charles Evans Research Award (O.E.B., J.D.B. and J.R.M.), the Wellcome Trust (WT095908 (P.F.) and WT098051), the Canadian Institutes of Health Research (MOP74667 (J.P.R.)) and the Natural Sciences and Engineering Research Council of Canada (312221 (J.P.R.)). Author Contributions: J.J.S. developed the assembly, coordinated analyses, performed analyses of genome structure and conserved synteny, coordinated the manuscript, and wrote and edited the manuscript. S.K. contributed to analyses of GC content, assembly completeness, vertebrate-specific genes, myelin-related genes and limb development, and to preparation of the manuscript and supplements. C.H. compiled molecular data sets and developed the consortium gene annotations and annotation pipeline. T.S.-S. developed the protocol for the preparation of BACs, identified the sequenced individual, and prepared genomic DNA for sequencing and BAC library construction. N.J. performed computational identification and analysis of transposable elements. M.D.Y. and M.S.C. contributed to the development of the consortium gene annotations and the annotation pipeline. T.M. and A.M. performed analysis of vertebrate-specific gene families, codon usage bias and amino-acid composition, and contributed to the writing of the manuscript. S.D. and M.H. contributed to analysis of codon usage bias and amino-acid composition. O.E.B., J.R.M., J.D.B. and R.S. performed experiments generating neuronal transcriptomes and data, and sequence analysis related to the vertebrate central nervous system. C.S., L.M.W., A.S.G., M.C. and R.K. performed experiments and data analysis related to the identification and annotation of Hox genes, led and prepared by L.M.W. S.A.S., W.A.D. and J.A.H. performed analyses related to the evolution of neuroendocrine genes, led by S.A.S. and prepared by W.A.D. C.T.A., N.R.S., K.M.B., J.P.R., S.D. and M.H. performed analyses related to the evolution of immune system genes, led and prepared by C.T.A., K.M.B., J.P.R. and M.H. N.R. and C.J.T. performed analyses related to the evolution and development of appendages. P.P. performed BLAST analyses of the noncoding portion of the lamprey genome, and G.E. analyzed BLAST output and wrote the corresponding sections. M.R., B.L.A. and S.M.J.S. developed the Ensembl gene set, led and prepared by M.R. M.M., M.P. and J.H. performed GeneTree and CAFE analysis for the study of whole-genome duplications at the stem of the vertebrate lineage and prepared the corresponding sections. T.S.-S., M.J., J.A.L. and D.W.M. developed the protocol for the preparation of cDNA. N.M. and P.G. provided isolated leukocyte RNA. C.T.B. and K.G.N. performed transcriptome assemblies. W.L., Y.-W.C.-D., S.V.L., C.-Y.Y. and D.W.M. contributed to next-generation transcriptome sequencing. Z.P. provided lamprey leukocyte RNA and cDNA samples and libraries, and evaluated the first draft assembly of the genome. B.F. contributed to the development of neurodevelopment-related text. P.J.d.J. and B.Z. generated the BAC library used for genome sequencing and assembly. L.L.F., W.C.W. and S.W.C. contributed to sequencing project management. B.T. coordinated the cDNA sequencing projects. P.F. supervised the Ensembl annotation efforts. M.E.B. contributed to the conception of the sea lamprey genome project and the development of the manuscript. R.K.W. provided supervision of the genome sequencing project. W.L. provided coordination of the consortium and analysis of the assembly, and contributed to the development of the manuscript. COMPETING FINANCIAL INTERESTS The authors declare no competing financial interests.

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