Skip to main content
Log in

Complete Mitochondrial DNA Sequence of the Eastern Oyster Crassostrea virginica

  • Published:
Marine Biotechnology Aims and scope Submit manuscript

Abstract

The complete mitochondrial genome of the eastern oyster Crassostrea virginica (GenBank accession number AY905542) is 17,243 bp in length and contains 2 ribosomal genes, 12 protein-coding genes, and 23 transfer RNAs. The arrangement of protein-coding genes is identical to that of the congeneric Pacific oyster C. gigas, but tRNA genes show several duplications and extensive rearrangements between the species. Unique features in C. virginica include an additional trnM gene, the absence of an ATPase subunit 8 (atp8) gene, and an inferred translational frameshift within the cytochrome b (cob) gene. In both species the large subunit ribosomal RNA gene is encoded by 2 separate regions of the mitochondrial genome, the first reported case of a split ribosomal RNA gene in a metazoan. Translation of protein-coding genes in both species is initiated with methionine, with the exception of cob, which uses leucine. In C. virginica translation of all protein-coding genes (except possibly cob) terminates with TAA, with polyadenylation completing the primary transcript in cytochrome oxidase subunit III (cox3) and NADH dehydrogenase subunit 4L (nad4L), whereas C. gigas employs stop codons TAA and TAG equally. Interspecific divergence of mitochondrially encoded proteins is considerable, with amino acid identities ranging from 47% to 92%. A single major noncoding region representing the putative control region is found in both species.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  • Avise JC (2000). Phylogeography: The History and Formation of Species. (Cambridge, Mass: Harvard University Press)

    Google Scholar 

  • Beaudoing E, Gautheret D (2001) Identification of alternate polyadenylation sites and analysis of their tissue distribution using EST data. Genome Res 11: 1520–1526

    Article  Google Scholar 

  • Beckenbach AT, Robson SKA, Crozier RH (2005) Single nucleotide +1 frameshifts in an apparently functional mitochondrial cytochrome b gene in ants of the genus Polyrhachis. J Mol Evol 60: 141–152

    Article  Google Scholar 

  • Boore JL (1999) Animal mitochondrial genomes. Nucleic Acids Res 27: 1767–1780

    Article  Google Scholar 

  • Boore JL, Brown WM (1994) Complete DNA sequence of the mitochondrial genome of the black chiton, Katharina tunicata. Genetics 138: 423–443

    Google Scholar 

  • Boore JL, Medina M Rosenberg LA (2004) Complete sequences of the highly rearranged molluscan mitochondrial genomes of the scaphopod Graptacme eborea and the bivalve Mytilus edulis. Mol Biol Evol 21: 1492–1503

    Google Scholar 

  • Brown WM, (1985) The mitochondrial genome of animals. In: Molecular Evolutionary Genetics, MacIntyre RJ (ed). (New York, NY: Plenum Press), pp 95–130

    Google Scholar 

  • Cannone JJ, Subramanian S, Schnare MN, Collett JR, D’Souza LM, Du Y, Feng B, Lin N, Madabusi LV, Muller KM, Pande N, Shang Z, Yu N, Gutell RR (2002). The Comparative RNA Web (CRW) Site: An online database of comparative sequence and structure information for ribosomal, intron, and other RNAs. BioMed Central Bioinformatics 3: 2

    Google Scholar 

  • Cardon LR, Burge C, Clayton DW, Karlin S (1994) Pervasive CpG suppression in animal mitochondrial genomes. Proc Natl Acad Sci USA 91: 3799–3803

    Google Scholar 

  • Farabaugh PJ (1996) Programmed translational frameshifting. Annu Rev Genet 30, 507–528

    Article  Google Scholar 

  • Gissi C, Pesole G (2003) Transcript mapping and genome annotation of ascidian mtDNA using EST data. Genome Res 13: 2203–2212

    Article  Google Scholar 

  • Gissi C, Iannelli F, Pesole G (2004) Complete mtDNA of Ciona intestinalis reveals extensive gene rearrangement and the presence of an atp8 and an extra trnM gene in ascidians. J Mol Evol 58: 376–389

    Article  Google Scholar 

  • Gueguen Y, Cadoret JP, Flament D, Barreau-Roumiguière C, Girardot AL, Garniera J, Hoareaua A, Bachère E, Escoubas JM (2003) Immune gene discovery by expressed sequence tags generated from hemocytes of the bacteria-challenged oyster, Crassostrea gigas. Gene 303: 139–145

    Article  Google Scholar 

  • Helfenbein KG, Brown WM, Boore JL (2001) The complete mitochondrial genome of the articulate brachiopod Terebratalia transversa. Mol Biol Evol 18: 1734–1744

    Google Scholar 

  • Hoffmann RJ, Boore JL, Brown WM (1992). A novel mitochondrial genome organization for the blue mussel, Mytilus edulis. Genetics 131: 397–412

    Google Scholar 

  • Jameson D, Gibson AP, Hudelot C, Higgs PG (2003) OGRe: a relational database for comparative analysis of mitochondrial genomes. Nucleic Acids Res 31: 202–206

    Article  Google Scholar 

  • Jenny MJ, Ringwood AH, Lacy ER, Lewitus AJ, Kempton JW, Gross PS, Warr GW, Chapman RW (2002) Potential indicators of stress response identified by expressed sequence tag analysis of hemocytes and embryos from the American oyster, Crassostrea virginica. Mar Biotechnol 4: 81–93

    Article  Google Scholar 

  • Kuwahara R, Oohara I (2001). Variability of two major non-coding regions of the Japanese oyster Crassostrea gigas mitochondrial DNA. Bull Nat Res Inst Fish Sci 16: 97–101

    Google Scholar 

  • Lowe TM, Eddy SR (1997) tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Res 25: 955–964

    Article  Google Scholar 

  • Milbury CA, (2003) Using mitochondrial DNA markers to monitor oyster stock enhancement in the Choptank River, Chesapeake Bay. M.S. thesis, College of Marine Studies, University of Delaware, Lewes

  • Milbury CA, Gaffney PM, Meritt DW, Newell RIE (2004) Mitochondrial DNA markers allow monitoring of oyster stock enhancement in the Chesapeake Bay. Mar Biol 145: 351–359

    Article  Google Scholar 

  • Mindell DP, Sorenson MD, Dimcheff DE (1998) An extra nucleotide is not translated in mitochondrial ND3 of some birds and turtles. Mol Biol Evol 15: 1568–1571

    Google Scholar 

  • Newell RIE (1988). Ecological changes in Chesapeake Bay: are they the result of overharvesting the American oyster, Crassostrea virginica? In: Understanding the Estuary: Advances in Chesapeake Bay Research, Vol. 129, Lynch MP, Krome EC (eds). (Gloucester Point, VA: Chesapeake Research Consortium) pp 536–546

    Google Scholar 

  • Peatman EJ, Wei X, Feng J, Liu LL, Kucuktas H, Li P, He C, Rouse D, Wallace R, Dunham R, Liu Z (2004). Development of expressed sequence tags from eastern oyster (Crassostrea virginica): lessons learned from previous efforts. Mar Biotechnol 6S, 491–496

    Google Scholar 

  • Perna NT, Kocher TD (1995) Patterns of nucleotide composition at fourfold degenerate sites of animal mitochondrial genomes. J Mol Evol 41: 353–358

    Google Scholar 

  • Rafferty GP, Powell R (2002) Identification of genes expressed in the gill tissue of the Pacific oyster (Crassostrea gigas) using expressed-sequence tags. J Mollusc Stud 68: 397-399

    Google Scholar 

  • Rawlings TA, Collins TM, Bieler R (2001) A major mitochondrial gene rearrangement among closely related species. Mol Biol Evol 18: 1604–1609

    Google Scholar 

  • Reeb CA, Avise JC (1990) A genetic discontinuity in a continuously distributed species: mitochondrial DNA in the American oyster, Crassostrea virginica. Genetics 124: 397–406

    Google Scholar 

  • Roberti M, Polosa PL, Bruni F, Musicco C, Gadaleta MN, Cantatore P (2003). DmTTF, a novel mitochondrial transcription termination factor that recognises two sequences of Drosophila melanogaster mitochondrial DNA. Nucleic Acids Res 31: 1597–1604

    Article  Google Scholar 

  • Rothschild BJ, Ault JS, Goulletquer P, Héral M (1994). Decline of the Chesapeake Bay oyster population: a century of habitat destruction and overfishing. Mar Ecol Prog Ser 111: 29–39

    Google Scholar 

  • Serb JM, Lydeard C (2003) Complete mtDNA sequence of the North American freshwater mussel, Lampsilis ornata (Unionidae): An examination of the evolution and phylogenetic utility of mitochondrial genome organization in Bivalvia (Mollusca). Mol Biol Evol 20: 1854–1866

    Google Scholar 

  • Shearer TL, Van Oppen MJH, Romano SL, Wörheide G (2002) Slow mitochondrial DNA sequence evolution in the Anthozoa (Cnidaria). Oceanogr Mar Biol Annu Rev 11: 2475–2487

    Google Scholar 

  • Stothard P (2000) The Sequence Manipulation Suite: JavaScript programs for analyzing and formatting protein and DNA sequences. BioTechniques 28: 1102–1104

    Google Scholar 

  • Valverde JR, Marco R, Garesse R (1994) A conserved heptamer motif for ribosomal RNA transcription termination in animal mitochondria. Proc Natl Acad Sci USA 91: 5368–5371

    Google Scholar 

  • Wakefield JR, Gaffney PM (1996). DGGE reveals additional population structure in American oyster (Crassostrea virginica) populations. J Shellfish Res 15: 513

    Google Scholar 

  • Wolstenholme DR (1992) Animal mitochondrial DNA: structure and evolution. Int Rev Cytol 141: 173–216

    Google Scholar 

  • Wolstenholme D, MacFarlane JL, Okimoto R, Clary DO, Wahleithner JA (1987) Bizarre tRNAs inferred from DNA sequences of mitochondrial genomes of nematode worms. Proc Natl Acad Sci USA 84: 1324–1328

    Google Scholar 

  • Wyman SK, Jansen RK, Boore JL (2004) Automatic annotation of organellar genomes with DOGMA. Bioinformatics 20: 3252–3254

    Article  Google Scholar 

  • Yokobori SI, Fukuda N, Nakamura M, Aoyama T, Oshima T (2004) Long-term conservation of six duplicated structural genes in cephalopod mitochondrial genomes. Mol Biol Evol 21: 2034–2046

    Google Scholar 

Download references

Acknowledgments

We thank Robin Gutell and Jamie Cannone for assistance in discovering the split rrnL gene, and Jeffrey Boore for help in analyzing the cob translational frameshifting. This work was supported by Delaware Sea Grant and the NOAA Oyster Disease Research Program.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Patrick M. Gaffney.

Appendix

Appendix

  Electronic Appendix A. Primers Used to Amplify Large Fragments of Crassostrea virginica Mitochondrial Genome
  Electronic Appendix B. Primers Used to Sequence Crassostrea virginica Mitochondrial genome
  Electronix Appendix C. Codon Usage in Crassostrea virginica and C. gigas Mitochondrial genomes

Rights and permissions

Reprints and permissions

About this article

Cite this article

Milbury, C.A., Gaffney, P.M. Complete Mitochondrial DNA Sequence of the Eastern Oyster Crassostrea virginica. Mar Biotechnol 7, 697–712 (2005). https://doi.org/10.1007/s10126-005-0004-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10126-005-0004-0

Keywords

Navigation