The Genome of the Sea Urchin Strongylocentrotus purpuratus

Sea Urchin Genome Sequencing Consortium, Erica Sodergren^1,2, George M. Weinstock^1,2*, Eric H Davidson³, R. Andrew Cameron³, Richard A. Gibbs^1,2, Robert C. Angerer⁴, Lynne M. Angerer⁴, Maria Ina Arnone⁵, David R. Burgess⁶, Robert D. Burke⁷, James A. Coffman⁸, Michael Dean⁹, Maurice R. Elphick¹⁰, Charles A. Ettensohn¹¹, Kathy R. Foltz¹², Amro Hamdoun¹³, Richard O. Hynes¹⁴, William H. Klein¹⁵, William Marzluff¹⁶, David R. McClay¹⁷, Robert L. Morris¹⁸, Arcady Mushegian^19,20, Jonathan P. Rast²¹, L. Courtney Smith²², Michael C. Thorndyke²³, Victor D. Vacquier²⁴, Gary M. Wessel²⁵, Greg Wray²⁶, Lan Zhang^1,2, Christine G. Elsik²⁷, Olga Ermolaeva²⁸, Wratko Hlavina²⁸, Gretchen Hofmann²⁹, Paul Kitts²⁸, Melissa J. Landrum²⁸, Aaron J. Mackey³⁰, Donna Maglott²⁸, Georgia Panopoulou³¹, Albert J. Poustka³¹, Kim Pruitt²⁸, Victor Sapojnikov²⁸, Xingzhi Song^1,2, Alexandre Souvorov²⁸, Victor Solovyev³², Zheng Wei⁴, Charles A. Whittaker³³, Kim Worley^1,2, K. James Durbin^1,2, Yufeng Shen^1,2, Olivier Fedrigo²⁶, David Garfield²⁶, Ralph Haygood¹⁷, Alexander Primus²⁶, Rahul Satija²⁶, Tonya Severson²⁶, Manuel L. Gonzalez-Garay^1,2, Andrew R. Jackson^1,2, Aleksandar Milosavljevic^1,2, Mark Tong^1,2, Christopher E. Killian³⁴, Brian T. Livingston³⁵, Fred H. Wilt³⁴, Nikki Adams³⁵, Robert Bellé^36,37, Seth Carbonneau⁸, Rocky Cheung¹⁶, Patrick Cormier^36,37, Bertrand Cosson^36,37, Jenifer Croce¹⁷, Antonio Fernandez-Guerra^38,39, Anne-Marie Genevière^38,39, Manisha Goel¹⁹, Hemant Kelkar⁴⁰, Julia Morales^36,37, Odile Mulner-Lorillon^36,37, Anthony J. Robertson⁸, Jared V. Goldstone⁴¹, Bryan Cole¹³, David Epel¹³, Bert Gold⁹, Mark E. Hahn⁴², Meredith Howard-Ashby³, Mark Scally⁹, John J. Stegeman⁴¹, Erin L. Allgood¹⁸, Jonah Cool¹⁸, Kyle M. Judkins¹⁸, Shawn S. McCafferty¹⁸, Ashlan M. Musante¹⁸, Robert A. Obar⁴², Amanda P. Rawson¹⁸, Blair J. Rossetti¹⁸, Ian R. Gibbons⁴³, Matthew P. Hoffman⁶, Andrew Leone⁶, Sorin Istrail⁴⁴, Stefan C. Materna³, Manoj P. Samanta^45,46, Viktor Stolc⁴⁵, Waraporn Tongprasit⁴⁵, Qiang Tu³, Karl-Frederik Bergeron⁴⁷, Bruce P. Brandhorst⁴⁸, James Whittle⁴⁹, Kevin Berney³, David J. Bottjer⁵⁰, Cristina Calestani⁵¹, Kevin Peterson⁵², Elly Chow⁵³, Qiu Autumn Yuan⁵³, Eran Elhaik⁵⁴, Dan Graur⁵⁴, Justin T. Reese²⁷, Ian Bosdet⁵⁵, Shin Heesun⁵⁵, Marco A. Marra⁵⁵, Jacqueline Schein⁵⁵, Michele K. Anderson⁵⁶, Virginia Brockton²², Katherine M. Buckley²², Avis H. Cohen⁵⁷, Sebastian D. Fugmann⁵⁸, Taku Hibino²¹, Mariano Loza-Coll²¹, Audrey J. Majeske²², Cynthia Messier²¹, Sham V. Nair⁵⁹, Zeev Pancer⁶⁰, David P. Terwilliger²², Cavit Agca⁶¹, Enrique Arboleda⁵, Nansheng Chen⁴⁸, Allison M. Churcher⁶², F. Hallböök⁶³, Glen W. Humphrey⁶⁴, Mohammed M. Idris⁵, Takae Kiyama¹⁵, Shuguang Liang¹⁵, Dan Mellott⁶⁰, Xiuqian Mu¹⁵, Greg Murray⁴⁶, Robert P. Olinski⁶³, Florian Raible^65,66, Matthew Rowe¹⁰, John S. Taylor⁶², Kristin Tessmar-Raible⁶⁵, D. Wang⁶², Karen H. Wilson²³, Shunsuke Yaguchi⁷, Terry Gaasterland²⁴, Blanca E. Galindo⁶⁷, Herath J. Gunaratne²⁴, Celina Juliano²⁵, Masashi Kinukawa²⁴, Gary W. Moy²⁴, Anna T. Neill²⁴, Mamoru Nomura²⁴, Michael Raisch¹², Anna Reade¹², Michelle M. Roux¹², Jia L. Song²⁵, Yi-Hsien Su³, Ian K. Townley¹², Ekaterina Voronina²⁵, Julian L. Wong²⁵, Gabriele Amore⁵, Margherita Branno⁵, Euan R. Brown⁵, Vincenzo Cavalieri⁶⁸, Véronique Duboc⁶⁹, Louise Duloquin⁶⁹, Constantin Flytzanis^70,71, Christian Gache⁶⁹, François Lapraz⁶⁹, Thierry Lepage⁶⁹, Annamaria Locascio⁵, Pedro Martinez^72,73, Giorgio Matassi⁷⁴, Valeria Matranga⁷⁵, Ryan Range⁶⁹, Francesca Rizzo⁵, Eric Röttinger⁶⁹, Wendy Beane¹⁷, Cynthia Bradham¹⁷, Christine Byrum^17,76, Tom Glenn¹⁷, Sofia Hussain⁷⁷, Gerard Manning⁷⁸, Esther Miranda¹⁷, Rebecca Thomason^17,76, Katherine Walton¹⁷, Athula Wikramanayke⁷⁶, Shu-Yu Wu¹⁷, Ronghui Xu⁷⁶, C. Titus Brown³, Lili Chen³, Rachel F. Gray³, Pei Yun Lee³, Jongmin Nam³, Paola Oliveri³, Joel Smith³, Donna Muzny^1,2, Stephanie Bell^1,2, Joseph Chacko^1,2, Andrew Cree^1,2, Stacey Curry^1,2, Clay Davis^1,2, Huyen Dinh^1,2, Shannon Dugan-Rocha^1,2, Jerry Fowler^1,2, Rachel Gill^1,2, Cerrissa Hamilton^1,2, Judith Hernandez^1,2, Sandra Hines^1,2, Jennifer Hume^1,2, LaRonda Jackson^1,2, Angela Jolivet^1,2, Christie Kovar^1,2, Sandra Lee^1,2, Lora Lewis^1,2, George Miner^1,2, Margaret Morgan^1,2, Lynne V. Nazareth^1,2, Geoffrey Okwuonu^1,2, David Parker^1,2, Ling-Ling Pu^1,2, Rachel Thorn^1,2, Rita Wright^1,2

¹ Human Genome Sequencing Center, Baylor College of Medicine, One Baylor Plaza, Houston, TX 77030, USA.
² Department of Molecular and Human Genetics, Baylor College of Medicine, One Baylor Plaza, Houston, TX 77030, USA.
³ Division of Biology, California Institute of Technology, Pasadena, CA 91125, USA.
⁴ National Institute of Dental and Craniofacial Research, National Institutes of Health (NIH), Bethesda, MD 20892, USA.
⁵ Stazione Zoologica Anton Dohrn, Villa Comunale, 80121 Napoli, Italy.
⁶ Department of Biology, Boston College, Chestnut Hill, MA 02467, USA.
⁷ Department of Biology, Department of Biochemistry and Microbiology, University of Victoria, Victoria, BC, Canada, V8W 3N5.
⁸ Mount Desert Island Biological Laboratory, Salisbury Cove, ME 04672, USA.
⁹ Human Genetics Section, Laboratory of Genomic Diversity, National Cancer Institute–Frederick, Frederick, MD 21702, USA.
¹⁰ School of Biological and Chemical Sciences, Queen Mary, University of London, London E1 4NS, UK.
¹¹ Department of Biological Sciences, Carnegie Mellon University, Pittsburgh, PA, 15213, USA.
¹² Department Molecular, Cellular and Developmental Biology and the Marine Science Institute, University of California, Santa Barbara, Santa Barbara, CA 93106–9610, USA.
¹³ Hopkins Marine Station, Stanford University, Pacific Grove, CA 93950, USA.
¹⁴ Howard Hughes Medical Institute, Center for Cancer Research, Massachusetts Institute of Technology (MIT), Cambridge, MA 02139, USA.
¹⁵ Departments of Biochemistry and Molecular Biology, University of Texas, M.D.Anderson Cancer Center, Houston, TX, 77030, USA.
¹⁶ Molecular Biology and Biotechnology, University of North Carolina at Chapel Hill, Chapel Hill, NC 27599, USA.
¹⁷ Department of Biology, Duke University, Durham, NC 27708, USA.
¹⁸ Department of Biology, Wheaton College, Norton, MA 02766, USA.
¹⁹ Stowers Institute for Medical Research, Kansas City, MO 64110, USA.
²⁰ Department of Microbiology, Kansas University Medical Center, Kansas City, KS 66160, USA.
²¹ Sunnybrook Research Institute and Department of Medical Biophysics, University of Toronto, Toronto, Ontario, Canada, M4N 3M5.
²² Department of Biological Sciences, George Washington University, Washington, DC 20052, USA.
²³ Royal Swedish Academy of Sciences, Kristineberg Marine Research Station, Fiskebackskil, 450 34, Sweden.
²⁴ Marine Biology, Scripps Institution of Oceanography, University of California San Diego, La Jolla, CA 92093–0202, USA.
²⁵ Department of Molecular and Cellular Biology and Biochemistry, Brown University Providence, RI 02912, USA.
²⁶ Department of Biology and Institute for Genome Sciences and Policy, Duke University, Durham, NC 27708, USA.
²⁷ Department of Animal Science, Texas A&M University, College Station, TX 77843, USA.
²⁸ National Center for Biotechnology Information, National Library of Medicine, NIH, Bethesda, MD 20894, USA.
²⁹ Department of Ecology, Evolution, and Marine Biology, University of California Santa Barbara, Santa Barbara, CA 93106, USA.
³⁰ Penn Genomics Institute, University of Pennsylvania, Philadelphia, PA 19104, USA.
³¹ Evolution and Development Group, Max-Planck Institut fuer Molekulare Genetik, 14195 Berlin, Germany.
³² Royal Holloway, University of London, Egham, Surrey TW20 0EX, UK.
³³ Center for Cancer Research, MIT, Cambridge, MA 02139, USA.
³⁴ Department of Molecular and Cell Biology, University of California, Berkeley, Berkeley, CA 94720–3200, USA.
³⁵ Biology Department, California Polytechnic State University, San Luis Obispo, CA 93407, USA.
³⁶ Université Pierre et Marie Curie-Paris6, UMR 7150, Equipe Cycle Cellulaire et Développement, Station Biologique de Roscoff, 29682 Roscoff Cedex, France.
³⁷ CNRS, UMR 7150, Station Biologique de Roscoff, 29682 Roscoff Cedex, France.
³⁸ CNRS, UMR7628, Banyuls-sur-Mer, F-66650, France.
³⁹ Université Pierre et Marie Curie-Paris 6, UMR7628, Banyuls-sur-Mer, F-66650, France.
⁴⁰ Center for Bioinformatics, University of North Carolina at Chapel Hill, Chapel Hill, NC 27599, USA.
⁴¹ Biology Department, Woods Hole Oceanographic Institution, Woods Hole, MA 02543, USA.
⁴² Tethys Research, LLC, 2115 Union Street, Bangor, Maine 04401, USA.
⁴³ Department of Molecular, Cellular, and Developmental Biology, University of California, Berkeley, Berkeley, CA 94720, USA.
⁴⁴ Center for Computational Molecular Biology, and Computer Science Department, Brown University, Providence, RI 02912, USA.
⁴⁵ Genome Research Facility, National Aeronautics and Space Administration, Ames Research Center, Moffet Field, CA 94035, USA.
⁴⁶ Systemix Institute, Cupertino, CA 95014, USA.
⁴⁷ Department of Molecular Biology and Biochemistry, Simon Fraser University, Burnaby, British Columbia, Canada, V5A 1S6.
⁴⁸ Department of Molecular Biology and Biochemistry, Simon Fraser University, Burnaby, BC, Canada, V5A 1S6.
⁴⁹ Department of Biology, Center for Cancer Research, MIT, Cambridge, MA 02139, USA.
⁵⁰ Department of Earth Sciences, University of Southern California, Los Angeles, CA 90089–0740, USA.
⁵¹ Department of Biology, University of Central Florida, Orlando, FL 32816–2368, USA.
⁵² Department of Biological Sciences, Dartmouth College, Hanover, NH 03755, USA.
⁵³ Center for Computational Regulatory Genomics, Beckman Institute, California Institute of Technology, Pasadena, CA 91125, USA.
⁵⁴ Department of Biology and Biochemistry, University of Houston, Houston, TX 77204, USA.
⁵⁵ Genome Sciences Centre, British Columbia Cancer Agency, Vancouver, BC, Canada, V5Z 4E6.
⁵⁶ Department of Immunology, University of Toronto, Toronto, Ontario, Canada, M4N 3M5.
⁵⁷ Department of Biology and the Institute of Systems Research, University of Maryland, College Park, MD 20742, USA.
⁵⁸ Laboratory of Cellular and Molecular Biology, National Institute on Aging, NIH, Baltimore, MD 21224, USA.
⁵⁹ Department of Biological Sciences, Macquarie University, Sydney NSW 2109, Australia.
⁶⁰ Center of Marine Biotechnology, UMBI, Columbus Center, Baltimore, MD 21202, USA.
⁶¹ Department of Cell Biology and Anatomy, Louisiana State University Health Sciences Center, New Orleans, LA 70112, USA.
⁶² Department of Biology, University of Victoria, Victoria, BC, Canada, V8W 2Y2.
⁶³ Department of Neuroscience, Uppsala University, Uppsala, Sweden.
⁶⁴ Laboratory of Cellular and Molecular Biophysics, National Institute of Child Health and Development, NIH, Bethesda, MD 20895, USA.
⁶⁵ Developmental Unit, EMBL, 69117 Heidelberg, Germany.
⁶⁶ Computational Unit, EMBL, 69117 Heidelberg, Germany.
⁶⁷ Biotechnology Institute, Universidad Nacional Autónoma de Mexico (UNAM), Cuernavaca, Morelos, Mexico 62250.
⁶⁸ Department of Cellular and Developmental Biology "Alberto Monroy," University of Palermo, 90146 Palermo, Italy.
⁶⁹ Laboratoire de Biologie du Développement (UMR 7009), CNRS and Université Pierre et Marie Curie (Paris 6), Observatoire Océanologique, 06230 Villefranche-sur-Mer, France.
⁷⁰ Department of Biology, University of Patras, Patras, Greece.
⁷¹ Department of Molecular and Cellular Biology, Baylor College of Medicine, One Baylor Plaza, Houston, TX 77030, USA.
⁷² Departament de Genetica, Universitat de Barcelona, 08028–Barcelona, Spain.
⁷³ Institució Catalana de Recerca i Estudis Avancats (ICREA), Barcelona, Spain.
⁷⁴ Institut Jacques Monod, CNR-UMR 7592, 75005 Paris, France.
⁷⁵ Consiglio Nazionale delle Ricerche, Istituto di Biomedicina e Immunologia Molecolare "Alberto Monroy," 90146 Palermo, Italy.
⁷⁶ Department of Zoology, University of Hawaii at Manoa, Honolulu, HI 96822, USA.
⁷⁷ Department of Biology, University of South Florida, Tampa, FL 33618, USA.
⁷⁸ Razavi-Newman Center for Bioinformatics, Salk Institute for Biological Studies, La Jolla, CA 92186, USA.

Fig. 1. The phylogenetic position of the sea urchin relative to other model systems and humans. The chordates are shown on the darker blue background overlapping the deuterostomes as a whole on a lighter blue background. Organisms for which genome projects have been initiated or finished are shown across the top. [View Larger Version of this Image (18K GIF file)]

Fig. 2. Orthologs among the Bilateria. The number of 1:1 orthologs captured by BLAST alignments at a match value of e = 1 x 10–6 in comparisons of sequenced genomes among the Bilateria. The number of orthologs is indicated in the boxes along the arrows, and the total number of International Protein Index database sequences is shown under the species symbol. Hs, Homo sapiens; Mm, Mus musculus; Ci, Ciona intestinalis; Sp, S. purpuratus; Dm, Drosophila melanogaster; Ce, Caenorhabditis elegans. [View Larger Version of this Image (30K GIF file)]

Fig. 3. Protein kinase evolution: Invention and loss of protein kinase subfamilies in metazoan lineages. Deuterostomes share 9 protein kinase subfamilies absent from C. elegans and Drosophila, and the sea urchin has not lost any of the 158 metazoan primordial kinase classes, unlike insects or nematodes. [From (23)] [View Larger Version of this Image (9K GIF file)]

Fig. 4. Partial phylogenies of the Rho (A) and the Rab families (B) of small GTPases. The pink boxes highlight gene-specific duplications that increased sea urchin GTPase numbers, resulting in a complexity comparable to vertebrates. Numbers at each junction represent confidence values obtained via three independent phylogenetic methods [neighbor-joining (green), maximum parsimony (blue), and Bayesian (black)]; red stars indicate nodes retained by maximum likelihood. [From (28)] [View Larger Version of this Image (26K GIF file)]

Fig. 5. Survey of the Wnt family of secreted signaling molecules in selected metazoans. Each square indicates a single Wnt gene identified either through genome analyses or independent studies, and squares with a question mark indicate uncertainty of the orthology. Letter X's represent absence of members of that subfamily in the corresponding annotated genome; empty spaces have been left for species for which genomic databases are not yet available. [From (30)] [View Larger Version of this Image (23K GIF file)]

Fig. 6. Presence of Wnt signaling machinery components (A) and target genes (B) in the S. purpuratus genome. (A) The 126 genes involved in the transduction of the Wnt signals have been separated into four categories from the extracellular compartment to the nucleus. Sea urchin homologs are identified by the lighter shade (indicated by both the number and the percentage of homologs that were identified within the chart); the total number of known genes is indicated in the chart legend. (B) The 93 reported Wnt targets have been divided into three categories: signaling molecules, transcription factors, and cell adhesion molecules. Colors and numbers are as in (A). [View Larger Version of this Image (19K GIF file)]

Fig. 7. Gene families encoding important innate immune receptors and complement factors in animals with sequenced genomes. For some key receptor classes, gene numbers in the sea urchin exceeds other animals by more than an order of magnitude. Representative animals include H.s., Homo sapiens; C.i., Ciona intestinalis; S.p. Strongylocentrotus purpuratus; D.m. Drosophila melanogaster; and C.e. Caenorhabditis elegans. Indicated gene families include TLR, toll-like receptors; NLR, NACHT and leucine-rich repeat (LRR) domain–containing proteins similar to the vertebrate Nod/NALP genes; SRCR, Scavenger receptor cysteine-rich domain genes; PGRP, peptidoglycan recognition protein domain genes; and GNBP, Gram-negative binding proteins. C3/4/5, thioester proteins homologous to vertebrate C3, C4, and C5; Bf/C2, complement factors homologous to vertebrate C2 and factor B; C1q/MBP, homologs of vertebrate lectin pathway receptors; and Terminal pathway, homologs of vertebrate C6, C7, C8, and C9. SRCR gene statistics are given as domain number/gene number for multiple SRCR-containing proteins (numbers for C. intestinalis includes all SRCR proteins). Asterisk in the D. melanogaster C3/4/5 column is meant to denote the presence of related thioester genes (TEPs) and a true C3/4/5 homolog from another arthropod. +/– for C. intestinalis Terminal pathway column indicates the presence of genes with similarity to C6 only (Nonaka and Yoshizaki 2004). Phylogenetic relations among species are indicated by a cladogram at the left. [View Larger Version of this Image (13K GIF file)]