White Shark Genome Reveals Ancient Elasmobranch Adaptations Associated with Wound Healing and the Maintenance of Genome Stability

  • Nicholas J. Marra
  • , Michael J Stanhope
  • , Nathaniel K. Jue
  • , Minghui Wang
  • , Qi Sun
  • , Paulina D. Pavinski Bitar
  • , Vincent P. Richards
  • , Aleksey S. Komissarov
  • , Mike Rayko
  • , Sergey Kliver
  • , Bryce J. Stanhope
  • , Chuck Winkler
  • , Stephen James O'Brien
  • , Agostinho Antunes
  • , Salvador Jorgensen
  • , Mahmood S. Shivji

Research output: Contribution to journalArticlepeer-review

Abstract

The white shark ( Carcharodon carcharias ; Chondrichthyes, Elasmobranchii) is one of the most publicly recognized marine animals. Here we report the genome sequence of the white shark and comparative evolutionary genomic analyses to the chondrichthyans, whale shark (Elasmobranchii) and elephant shark (Holocephali), as well as various vertebrates. The 4.63-Gbp white shark genome contains 24,520 predicted genes, and has a repeat content of 58.5%. We provide evidence for a history of positive selection and gene-content enrichments regarding important genome stability-related genes and functional categories, particularly so for the two elasmobranchs. We hypothesize that the molecular adaptive emphasis on genome stability in white and whale sharks may reflect the combined selective pressure of large genome sizes, high repeat content, high long-interspersed element retrotransposon representation, large body size, and long lifespans, represented across these two species. Molecular adaptation for wound healing was also evident, with positive selection in key genes involved in the wound-healing process, as well as Gene Ontology enrichments in fundamental wound-healing pathways. Sharks, particularly apex predators such as the white shark, are believed to have an acute sense of smell. However, we found very few olfactory receptor genes, very few trace amine-associated receptors, and extremely low numbers of G protein-coupled receptors. We did however, identify 13 copies of vomeronasal type 2 (V2R) genes in white shark and 10 in whale shark; this, combined with the over 30 V2Rs reported previously for elephant shark, suggests this gene family may underlie the keen odorant reception of chondrichthyans.

Original languageAmerican English
Pages (from-to)4446-4455
Number of pages10
JournalProceedings of the National Academy of Sciences (PNAS)
Volume116
Issue number10
DOIs
StatePublished - Mar 5 2019

Bibliographical note

Publisher Copyright:
© 2019 National Academy of Sciences. All Rights Reserved.

Funding

ACKNOWLEDGMENTS. We thank Peter Schweitzer and the Cornell Genomics facility for sequencing; Alvaro Gonzalo Hernandez and the DNA Services Facility at the University of Illinois for mate-pair library sequencing; Christian Gates and Richard Graff of Illumina for donating supplies and facilitating genome scaffolding and transcriptome assembly; Marco Blancette, Margot Hartley, and Michael Vierra at Dovetail Genomics for completing final scaffolding of the genome; John Coller of the Stanford Functional Genomics Facility for sequencing; Conor Stanhope for assistance with Excel; Lisa Natanson, Paul Kanive, John O’Sullivan, Chris Lowe, and the California State University, Long Beach Shark Laboratory for assistance in sample collection; Kimberley Finnegan for laboratory assistance; and Robert Weiss for providing helpful comments on the manuscript. Major funding for this study was provided by grants from the Save Our Seas Foundation, with additional funding provided by the Guy Harvey Ocean Foundation, Hai Stiftung/Shark Foundation, and the Monterey Bay Aquarium. A.A. was partially supported by the Portuguese Foundation for Science and Technology and the European Regional Development Fund in the framework of the program PT2020, by the European Structural and Investment Funds through the Competitiveness and Internationalization Operational Program–COMPETE 2020, and by National Funds through the Foundation for Science and Technology under the projects PTDC/AAG-GLO/ 6887/2014 (POCI-01-0124-FEDER-016845) and NORTE-01-0145-FEDER-031774. S.J.O. was supported, in part, by St. Petersburg State University (Genome Russia Grant 1.52.1647.2016). A.K., M.R., and S.K. were supported by Russian Foundation for Basic Research Grants 17-00-00144 as part of 17-00-00148.

FundersFunder number
Hai Stiftung/Shark Foundation
Monterey Bay Aquarium
Guy Harvey Ocean Foundation
Fundação para a Ciência e a TecnologiaNORTE-01-0145-FEDER-031774, PTDC/AAG-GLO/ 6887/2014, POCI-01-0124-FEDER-016845
Fundação para a Ciência e a Tecnologia
Russian Foundation for Basic Research17-00-00148, 17-00-00144
Russian Foundation for Basic Research
Saint Petersburg State University1.52.1647.2016
Saint Petersburg State University
Save our Seas Foundation
European Regional Development Fund
Programa Operacional Temático Factores de Competitividade

    ASJC Scopus Subject Areas

    • General

    Keywords

    • Comparative genomics
    • Genome stability
    • Elasmobranch evolution
    • Genomic Instability
    • Proto-Oncogene Proteins/genetics
    • Wound Healing/genetics
    • Selection, Genetic
    • Phylogeny
    • DNA Transposable Elements
    • Genes, p53
    • Sharks/classification
    • Adaptation, Physiological/physiology
    • Animals
    • Genome

    Disciplines

    • Biology
    • Genetics and Genomics
    • Life Sciences
    • Marine Biology

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