Advertisement

The Bilatarian Sea Urchin and the Radial Starlet Sea Anemone Globins Share Strong Homologies with Vertebrate Neuroglobins

  • Xavier Bailly
  • Serge N. Vinogradov
Part of the Protein Reviews book series (PRON, volume 9)

Abstract

A 34 834-bp gene in the genome of the sea urchin Strongylocentrotus purpuratus (Echinodermata) consists of 34 exons and 33 introns, and encodes a 2252aa putative chimeric Hb, comprising an unidentifiable nonglobin N-terminal domain of ∼150aa and 16 globin domains (D1–D16) of ∼150aa, except for D2, which lacks helices G and H. The similarity between the globin domains varies from 39 to 51% identity: they are linked tightly to one another, with interdomain segments of 10aa or less. Alignment of the globin domains with other globins shows them to have a D helix and His residues at both the E7 and F8 locations. Intron insertions within the globin domains occur at canonical positions B12.2 and G7.0. Blastp searches with each of the 16 domains showed a strong sequence similarity with vertebrate neuroglobins and globin X, the Cnidarian Nematostella vectensis, and with single-domain bacterial globins. A Bayesian analysis of the S. purpuratus globins, the 7 single domain globins from the Cnidarian N. vectensis and 80 globins from several metazoan groups, indicated that the S. purpuratus and N. vectensis globins share a molecular affinity with vertebrate neuroglobins and globin X, while annelid, mollusc, crustacean, lamprey, hagfish and urochordate globins form a clade with vertebrate cytoglobins. The common molecular signatures and gene structures shared between a radial metazoan, S. purpuratus and vertebrate globins suggest these proteins could exhibit ancestral metazoan globin properties and predate the Radiata-Bilateria split. We assume modern eumetazoan globin families could have derived from such a putative globin plesiogene.

Keywords

Protein Data Bank Globin Gene Blastp Search Intron Loss Brittle Star 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Babenko, V. N., Rogozin, I. B., Mekhedov, S. L., and Koonin, E. V. 2004. Prevalence of intron gain over intron loss in the evolution of paralogous gene families. Nucleic Acids Res. 32:3724–3733.PubMedCrossRefGoogle Scholar
  2. Baker, S., and Terwilliger, N. B. 1993. Hemoglobin structure and function in the rat-tailed sea cucumber Paracaudina chilensis. Biol. Bull. 185:115–122.CrossRefGoogle Scholar
  3. Bishop, J., Vandergon, T., Green, D., Doeller, J., and Kraus, D. 1998. A high-affinity hemoglobin is expressed in the notochord of amphioxus, Branchiostoma californiense. Biol. Bull. 195:255–259.CrossRefGoogle Scholar
  4. Burmester, T., Weich, B., Reinhardt, S., and Hankeln, T. 2000. A vertebrate globin expressed in the brain. Nature 407:520–523.PubMedCrossRefGoogle Scholar
  5. Burmester, T., Ebner, B., Weich, B., and Hankeln, T. 2002. Cytoglobin: a novel globin type ubiquitously expressed in vertebrate tissues. Mol. Biol. Evol. 19:416–421.PubMedGoogle Scholar
  6. Burmester, T., Haberkamp, M., Mitz, S., Roesner, A., Schmidt, M., Ebner, B., Gerlach, F., Fuchs, C., and Hankeln, T. 2004. Neuroglobin and cytoglobin: genes, proteins and evolution. IUBMB Life 56:703–707.PubMedCrossRefGoogle Scholar
  7. Christensen, A., Colacino, J., and Bonaventura, C. 2003. Functional and biochemical properties of the hemoglobins of the burrowing brittle star Hemipholis elongata Say (Echinodermata, Ophiuroidea). Biol. Bull. 205:54–65.PubMedCrossRefGoogle Scholar
  8. Coleman, M., Matthews, C. M., and Trotman, C. N. 2001. Multimeric hemoglobin of the Australian brine shrimp Parartemia. Mol. Biol. Evol. 18:570–576.PubMedGoogle Scholar
  9. Ebner, B., Burmester, T., and Hankeln, T. 2003. Globin genes are present in Ciona intesti-nalis. Mol. Biol. Evol. 20:1521–1525.PubMedCrossRefGoogle Scholar
  10. Hardison, R. C. 1996. A brief history of hemoglobins: plant, animal, protist, and bacteria. Proc. Natl. Acad. Sci. U.S.A. 93:5675–5679.PubMedCrossRefGoogle Scholar
  11. Huelsenbeck, J. P., and Ronquist, F. 2001. MRBAYES: Bayesian inference of phylogenet-ic trees. Bioinformatics 17:754–755.PubMedCrossRefGoogle Scholar
  12. Keller, E. B., and Noon, W. A. 1984. Intron splicing: a conserved internal signal in introns of animal pre-mRNAs. Proc. Natl. Acad. Sci. U.S.A. 81:7417–7420.PubMedCrossRefGoogle Scholar
  13. Letunic, I., Copley, R. R., Pils, B., Pinkert, S., Schultz, J., and Bork, P. 2006. SMART 5: domains in the context of genomes and networks. Nucleic Acids Res. 34:D257–260.PubMedCrossRefGoogle Scholar
  14. Matthews, C. M., and Trotman, C. N. 1998. Ancient and recent intron stability in the Artemia hemoglobin gene. J. Mol. Evol. 47:763–771.PubMedCrossRefGoogle Scholar
  15. Mattick, J. S., and Gagen, M. J. 2001. The evolution of controlled multitasked gene networks: The role of introns and other noncoding RNAs in the development of complex organisms. Mol. Biol. Evol. 18:1611–1630.PubMedGoogle Scholar
  16. Mauri, F., Omnaas, J., Davidson, L., Whitfill, C., and Kitto, G. B. 1991. Amino acid sequence of a globin from the sea cucumber Caudina (Molpadia) arenicola. Biochim. Biophys. Acta 1078:63–67.PubMedGoogle Scholar
  17. McDonald, G. D., Davidson, L., and Kitto, G. B. 1992. Amino acid sequence of the coelomic C globin from the sea cucumber Caudina (Molpadia) arenicola. J. Protein Chem. 11:29–37.PubMedCrossRefGoogle Scholar
  18. Miller, D. J., Ball, E. E., and Technau, U. 2005. Cnidarians and ancestral genetic complexity in the animal kingdom. Trends Genet. 21:536–539.PubMedCrossRefGoogle Scholar
  19. Mitchell, D. T., Kitto, G. B., and Hackert, M. L. 1995. Structural analysis of monomeric hemichrome and dimeric cyanomet hemoglobins from Caudina arenicola. J. Mol. Biol. 251:421–431.PubMedCrossRefGoogle Scholar
  20. Mount, S. M. 1982. A catalogue of splice junction sequences. Nucleic Acid Res. 10: 459–472.PubMedCrossRefGoogle Scholar
  21. Nott, A., Hir, H. L., and Moore, M. J. 2004. Splicing enhances translation in mammalian cells: An additional function of the exon junction complex, Genes Dev. 18:210–222.PubMedCrossRefGoogle Scholar
  22. Putnam, N. H., Srivastava, M., Hellsten, U., Dirks, B., Chapman, J., Salamov, A., Terry, A., Shapiro, H., Lindquist, E., Kapitonov, V. V., Jurka, J., Genikhovich, G., Grigoriev, I. V., Lucas, S. M., Steele, R. E., Finnerty, J. R., Technau, U., Martindale, M. Q., and Rokhsar, D. S. 2007. Sea anemone genome reveals ancestral eumetazoan gene repertoire and genomic organization. Science 317:86–94.PubMedCrossRefGoogle Scholar
  23. Roesner, A., Fuchs, C., Hankeln, T., and Burmester, T. 2005. A globin of ancient evolutionary origin in lower vertebrates: evidence for two distinct globin families in animals. Mol. Biol. Eval. 22:12–20.CrossRefGoogle Scholar
  24. Ruiz-Trillo, L, Riutort, M., Littlewood, D. T., Herniou, E. A., and Baguna, J. 1999. Acoel flatworms: earliest extant bilaterian Metazoans, not members of Platyhelminthes. Science 283:1919–1923.PubMedCrossRefGoogle Scholar
  25. Schaffer, A. A., Aravind, L., Madden, T., Shavrin, S., Spourge, J., Wolf, Y., Koonin, E.V., and Altschul, S. F. 2001. Improving the accuracy of PSI-BLAST protein database searches with composition-based statistics and other refinements. Nucleic Acids Res. 29:2994–3005.PubMedCrossRefGoogle Scholar
  26. Sempere, L. F., Martinez, P., Cole, C., Baguna, J., and Peterson, K. J. 2007. Phylogenetic distribution of microRNAs supports the basal position of acoel flatworms and the polyphyly of Platyhelminthes. Evol. Dev. 9:409–415.PubMedGoogle Scholar
  27. Shi, J., Blundell, T., and Mizuguchi, K. 2001. FUGUE: sequence-structure homology recognition using environment-specific substitution tables and structure-dependent gap penalties. J. Mol. Biol. 310:243–257.PubMedCrossRefGoogle Scholar
  28. Sodergren, E., Weinstock, G. M., Davidson, E. H., Cameron, R. A., Gibbs, R. A., et al. 2006. The genome of the sea urchin Strongylocentrotus purpuratus. Science 314:941–952.PubMedCrossRefGoogle Scholar
  29. Sullivan, J. C., Ryan, J. F., Watson, J. A., Webb, J., Mullikin, J. C., Rokhsar, D., and Finnerty, J. R. 2006. StellaBase: the Nematostella vectensis Genomics Database. Nucleic Acids Res. 34:D495–499.PubMedCrossRefGoogle Scholar
  30. Sullivan, J. C., Reitzel, A. M., and Finnerty, J. R. 2006. A high percentage of introns in human genes were present early in animal evolution: evidence from the basal metazoan Nematostella vectensis. Genome Inform. 17:219–229.PubMedGoogle Scholar
  31. Suzuki, T. 1989. Amino acid sequence of a major globin from the sea cucumber Paracaudina chilensis. Biochim. Biophys. Acta 998:292–296.PubMedGoogle Scholar
  32. Vasil, V., Clancy, M., Ferl, R. J., Vasil, I. K., and Hannah, L.C. 1989. Increased gene expression by the first intron of maize Shrunken-1 locus in grass species. Plant Physiol. 91:1575–1579.PubMedCrossRefGoogle Scholar
  33. Vinogradov, S. N., Hoogewijs, D., Bailly, X., Arredondo-Peter, R., Gough, J., Guertin, M., Dewilde, S., Moens, L., and Vanfleteren, J. R., 2005. Three globin lineages belonging to two structural classes in genomes from the three kingdoms of life. Proc. Natl. Acad. Sci. U.S.A. 102:11385–11389.PubMedCrossRefGoogle Scholar
  34. Vinogradov, S. N., Hoogewijs, D., Bailly, X., Arredondo-Peter, R., Gough, J., Guertin, M., Dewilde, S., Moens, L., and Vanfleteren, J. R., 2006. A phylogenomic profile of globins. BMC Evol. Biol. 6:31–67.PubMedCrossRefGoogle Scholar
  35. Vinogradov, S. N., Hoogewijs, D., Bailly, X., Dewilde, S., Moens, L., and Vanfleteren, J. R. 2007. A model of globin evolution. Gene 398:132–142.PubMedCrossRefGoogle Scholar
  36. Zhang, J. 2003. Evolution by gene duplication: an update. Trends Ecol. Evol. 18:292–298.CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Italia 2008

Authors and Affiliations

  • Xavier Bailly
    • 1
  • Serge N. Vinogradov
    • 2
  1. 1.Station Biologique de RoscoffRoscoffFrance
  2. 2.Department of Biochemistry and Molecular BiologyWayne State University School of MedicineDetroitUSA

Personalised recommendations