White shark genome reveals ancient elasmobranch adaptations associated with wound healing and the maintenance of genome stability

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.

Electroreception in marine fishes: chondrichthyans

“…Undoubtedly, this line of research would benefit from sequencing the genomes of key elasmobranch species and detailed studies on the molecular mechanisms that underlie chondrichthyan electroreception. Currently, the genomic sequences are known for a handful of the nearly 1300 chondrichthyans including: the whale shark Rhincodon typus (Smith 1828) (Read et al, ), C. punctatum , cloudy catshark Scyliorhinus torazame (Tanaka 1908) (Hara et al, ) , white shark Carcharodon carcharias (Linnaeus 1758) (Marra et al, ) and elephant shark Callorhinchus milii (Bory de Saint‐Vincent 1823) (Venkatesh et al, ). Leucoraja erinacea is the nearest model elasmobranch species to date and the assembly of its genome is underway at http://www.skatebase.org (Wang et al, ).…”

A Beautiful Life: High Risk–High Payoff in Genetic Science

“…These papers dissected the genetic components of bird biology determining feather development, wing aerodynamics, bone density, olfactory reception, visual opsins, tooth loss, plumage coloration, and many other features. Today whole genome sequences have been accomplished for more than 300 vertebrate species, and my own group at the Theodosius Dobzhansky Center for Genome Bioinformatics in St. Petersburg has contributed to the annotation and analyses of many of these (32,(36)(37)(38)(39)(40)(41)(42)(43)(44)(45)(46)(47). Comparative genomics approaches to whole genome sequences are now being used to impute the genome rearrangements that punctuated the mammalian radiations (48).…”

All creatures great and small

“…Sharks’ abilities to rapidly heal wounds have been known for decades 6. How they do so largely remains a mystery, but the genome of the white shark, Carcharodon carcharias , recently provided tantalising clues to this species’ wound healing capability 7. Elasmobranchs, which include sharks, were the first creatures to develop adaptive immunity and may hold important clues about how our own adaptive immune systems may falter.…”