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Characterization of the heart transcriptome of the white shark (Carcharodon carcharias)

BACKGROUND: The white shark (Carcharodon carcharias) is a globally distributed, apex predator possessing physical, physiological, and behavioral traits that have garnered it significant public attention. In addition to interest in the genetic basis of its form and function, as a representative of th...

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Autores principales: Richards, Vincent P, Suzuki, Haruo, Stanhope, Michael J, Shivji, Mahmood S
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2013
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3832898/
https://www.ncbi.nlm.nih.gov/pubmed/24112713
http://dx.doi.org/10.1186/1471-2164-14-697
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author Richards, Vincent P
Suzuki, Haruo
Stanhope, Michael J
Shivji, Mahmood S
author_facet Richards, Vincent P
Suzuki, Haruo
Stanhope, Michael J
Shivji, Mahmood S
author_sort Richards, Vincent P
collection PubMed
description BACKGROUND: The white shark (Carcharodon carcharias) is a globally distributed, apex predator possessing physical, physiological, and behavioral traits that have garnered it significant public attention. In addition to interest in the genetic basis of its form and function, as a representative of the oldest extant jawed vertebrate lineage, white sharks are also of conservation concern due to their small population size and threat from overfishing. Despite this, surprisingly little is known about the biology of white sharks, and genomic resources are unavailable. To address this deficit, we combined Roche-454 and Illumina sequencing technologies to characterize the first transciptome of any tissue for this species. RESULTS: From white shark heart cDNA we generated 665,399 Roche 454 reads (median length 387-bp) that were assembled into 141,626 contigs (mean length 503-bp). We also generated 78,566,588 Illumina reads, which we aligned to the 454 contigs producing 105,014 454/Illumina consensus sequences. To these, we added 3,432 non-singleton 454 contigs. By comparing these sequences to the UniProtKB/Swiss-Prot database we were able to annotate 21,019 translated open reading frames (ORFs) of ≥ 20 amino acids. Of these, 19,277 were additionally assigned Gene Ontology (GO) functional annotations. While acknowledging the limitations of our single tissue transcriptome, Fisher tests showed the white shark transcriptome to be significantly enriched for numerous metabolic GO terms compared to the zebra fish and human transcriptomes, with white shark showing more similarity to human than to zebra fish (i.e. fewer terms were significantly different). We also compared the transcriptome to other available elasmobranch sequences, for signatures of positive selection and identified several genes of putative adaptive significance on the white shark lineage. The white shark transcriptome also contained 8,404 microsatellites (dinucleotide, trinucleotide, or tetranucleotide motifs ≥ five perfect repeats). Detailed characterization of these microsatellites showed that ORFs with trinucleotide repeats, were significantly enriched for transcription regulatory roles and that trinucleotide frequency within ORFs was lower than for a wide range of taxonomic groups including other vertebrates. CONCLUSION: The white shark heart transcriptome represents a valuable resource for future elasmobranch functional and comparative genomic studies, as well as for population and other biological studies vital for effective conservation of this globally vulnerable species.
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spelling pubmed-38328982013-11-20 Characterization of the heart transcriptome of the white shark (Carcharodon carcharias) Richards, Vincent P Suzuki, Haruo Stanhope, Michael J Shivji, Mahmood S BMC Genomics Research Article BACKGROUND: The white shark (Carcharodon carcharias) is a globally distributed, apex predator possessing physical, physiological, and behavioral traits that have garnered it significant public attention. In addition to interest in the genetic basis of its form and function, as a representative of the oldest extant jawed vertebrate lineage, white sharks are also of conservation concern due to their small population size and threat from overfishing. Despite this, surprisingly little is known about the biology of white sharks, and genomic resources are unavailable. To address this deficit, we combined Roche-454 and Illumina sequencing technologies to characterize the first transciptome of any tissue for this species. RESULTS: From white shark heart cDNA we generated 665,399 Roche 454 reads (median length 387-bp) that were assembled into 141,626 contigs (mean length 503-bp). We also generated 78,566,588 Illumina reads, which we aligned to the 454 contigs producing 105,014 454/Illumina consensus sequences. To these, we added 3,432 non-singleton 454 contigs. By comparing these sequences to the UniProtKB/Swiss-Prot database we were able to annotate 21,019 translated open reading frames (ORFs) of ≥ 20 amino acids. Of these, 19,277 were additionally assigned Gene Ontology (GO) functional annotations. While acknowledging the limitations of our single tissue transcriptome, Fisher tests showed the white shark transcriptome to be significantly enriched for numerous metabolic GO terms compared to the zebra fish and human transcriptomes, with white shark showing more similarity to human than to zebra fish (i.e. fewer terms were significantly different). We also compared the transcriptome to other available elasmobranch sequences, for signatures of positive selection and identified several genes of putative adaptive significance on the white shark lineage. The white shark transcriptome also contained 8,404 microsatellites (dinucleotide, trinucleotide, or tetranucleotide motifs ≥ five perfect repeats). Detailed characterization of these microsatellites showed that ORFs with trinucleotide repeats, were significantly enriched for transcription regulatory roles and that trinucleotide frequency within ORFs was lower than for a wide range of taxonomic groups including other vertebrates. CONCLUSION: The white shark heart transcriptome represents a valuable resource for future elasmobranch functional and comparative genomic studies, as well as for population and other biological studies vital for effective conservation of this globally vulnerable species. BioMed Central 2013-10-11 /pmc/articles/PMC3832898/ /pubmed/24112713 http://dx.doi.org/10.1186/1471-2164-14-697 Text en Copyright © 2013 Richards et al.; licensee BioMed Central Ltd. http://creativecommons.org/licenses/by/2.0 This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
spellingShingle Research Article
Richards, Vincent P
Suzuki, Haruo
Stanhope, Michael J
Shivji, Mahmood S
Characterization of the heart transcriptome of the white shark (Carcharodon carcharias)
title Characterization of the heart transcriptome of the white shark (Carcharodon carcharias)
title_full Characterization of the heart transcriptome of the white shark (Carcharodon carcharias)
title_fullStr Characterization of the heart transcriptome of the white shark (Carcharodon carcharias)
title_full_unstemmed Characterization of the heart transcriptome of the white shark (Carcharodon carcharias)
title_short Characterization of the heart transcriptome of the white shark (Carcharodon carcharias)
title_sort characterization of the heart transcriptome of the white shark (carcharodon carcharias)
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3832898/
https://www.ncbi.nlm.nih.gov/pubmed/24112713
http://dx.doi.org/10.1186/1471-2164-14-697
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