Skip to main content

Evolutionary Physiology of Oxygen Secretion in the Eye of Fishes of the Suborder Notothenioidei

  • Chapter
Dioxygen Binding and Sensing Proteins

Part of the book series: Protein Reviews ((PRON,volume 9))

Abstract

We wish to tackle a survey on the overall understanding of the molecular properties, biological occurrence, physiological role and evolutionary origin of Root-effect Hbs.

Because high-Antarctic notothenioids still have Hbs endowed with Root effect also when the choroid rete is absent, this function may undergo neutral selection. Moreover, the deleterious effects of acidosis can be prevented by increase in the buffering capacity of Hb. Alternatively, high Hb buffer values may be related to the lower Hb content in the blood of notothenioids. As Hb is the main non-bicarbonate buffer in many vertebrates, a decrease in its concentration may entail detrimental consequences for blood acid-base regulation, which could be overcome by an increase in the number of buffering amino-acid residues per molecule. Whether these residues are the cause of the reduced Root effect, or the consequence of altered selection pressure on Hb buffer properties once the Root effect was diminished, remains an open question.

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

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 129.00
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 169.00
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  • Acierno, R., Maffia, M., Rollo, M., and Storelli, C. 1997. Buffer capacity in the blood of the hemoglobinless Antarctic fish Chionodraco hamatus. Comp. Biochem. Physiol. A 118:989–992.

    Article  Google Scholar 

  • Berenbrink, M. 2006. Evolution of vertebrate haemoglobins: Histidine side chains, specific buffer value and Bohr effect. Respir. Physiol. Neurobiol. 154:165–184.

    Article  PubMed  CAS  Google Scholar 

  • Berenbrink, M. 2007. Historical reconstructions of evolving physiological complexity: O2 secretion in the eye and swimbladder of fishes. J. Exp. Biol. 209:1641–1652.

    Article  Google Scholar 

  • Berenbrink, M., Koldkjaer, P., Kepp, O., and Cossins, A. R. 2005. Evolution of oxygen secretion in fishes and the emergence of a complex physiological system. Science 307:1752–1757.

    Article  PubMed  CAS  Google Scholar 

  • Bonaventura, J., Gillen, R. G., and Riggs, A. 1974. The hemoglobin of the Crosspterygian fish, Latimeria chalumnae (Smith). Arch. Biochem. Biophys. 163:728–734.

    Article  PubMed  CAS  Google Scholar 

  • Brittain, T. 2005. Root effect hemoglobins. J. Inorg. Biochem. 99:120–129.

    Article  PubMed  CAS  Google Scholar 

  • Camardella, L., Caruso, C., D’Avino, R., di Prisco, G., Rutigliano, B., Tamburrini, M., Fermi, G., and Perutz, M. F. 1992. Haemoglobin of the Antarctic fish Pagothenia bernacchii. Amino acid sequence, oxygen equilibria and crystal structure of its carbon-monoxy derivative. J. Mol. Biol. 224:449–460.

    Article  PubMed  CAS  Google Scholar 

  • D’Avino, R., Caruso, C., Tamburrini, M., Romano, M., Rutigliano, B., Polverino de Laureto, P., Camardella, L., Carratore, V., and di Prisco, G. 1994. Molecular characterization of the functionally distinct hemoglobins of the Antarctic fish Trematomus newnesi. J. Biol. Chem. 269:9675–9681.

    PubMed  CAS  Google Scholar 

  • Dettaï, A., and Lecointre, G. 2004. In search for Notothenioid (Teleostei) relatives. Antarctic Sci. 16:71–85.

    Article  Google Scholar 

  • Dettaï, A., and Lecointre, G. 2005. Further support for the clades obtained by multiple molecular phylogenies in the acanthomorph bush. Comp. Rend.-Biol. 328:674–689.

    Article  CAS  Google Scholar 

  • di Prisco, G., Eastman, J. T., Giordano, D., Parisi, E., and Verde, C. 2007. Biogeography and adaptation of Notothenioid fish: hemoglobin function and globin-gene evolution. Gene 398:143–155.

    Article  PubMed  CAS  Google Scholar 

  • Eastman, J. T. 2006. Aspects of the morphology of phyletically basal bovichtid fishes of the Antarctic suborder Notothenioidei (Perciformes). Polar Biol. 29:754–763.

    Article  Google Scholar 

  • Eastman, J. T., and Lannoo, M. J. 2004. Brain and sense organ anatomy and histology in hemoglobinless Antarctic icefishes (Perciformes: Notothenioidei: Channichthyidae). J. Morphol. 260:117–140.

    Article  PubMed  Google Scholar 

  • Egginton, S. 1997. A comparison of the response to induced exercise in red-and white-blooded Antarctic fishes. J. Comp. Physiol. 167:129–134.

    CAS  Google Scholar 

  • Feller, G., Poncin, A., Aittaleb, M., Schyns, R., and Gerday, C. 1994. The blood proteins of the Antarctic icefish Channichthys rhinoceratus: biological significance and purification of the two main components. J. Comp. Physiol. B 109:89–97.

    Google Scholar 

  • Huber, F., and Braunitzer, G. 1989. The primary structure of electric ray haemoglobin (Torpedo marmorata). Bohr effect and phosphate interaction. Biol. Chem. Hoppe-Seyler 370:831–838.

    PubMed  CAS  Google Scholar 

  • Ito, N., Komiyama, N. H., and Fermi, G. 1995. Structure of deoxyhemoglobin of the Antarctic fish Pagothenia bernacchii with an analysis of the structural basis of the Root effect by comparison of the liganded and unliganded hemoglobin structures. J. Mol. Biol. 250:648–658.

    Article  PubMed  CAS  Google Scholar 

  • Lowe, T. E., and Wells, R. M. G. 1997. Exercise challenge in Antarctic fishes: do haema-tology and muscle metabolite levels limit swimming performance? Polar Biol. 17:211–218.

    Article  Google Scholar 

  • Maddison, D. R., Maddison, W. P. 2003. MacClade 4: Analysis of phylogeny and character evolution. Version 4.06. Sinauer Associates, Sunderland, MA.

    Google Scholar 

  • Mazzarella, L., D’Avino, R., di Prisco, G., Savino, C., Vitagliano, L., Moody, P. C. E., and Zagari, A. 1999. Crystal structure of Trematomus newnesi hemoglobin re-opens the Root effect question. J. Mol. Biol. 287:897–906.

    Article  PubMed  CAS  Google Scholar 

  • Mazzarella, L., Bonomi, G., Lubrano, M., Merlino, A., Riccio, A., Vergara, A., Vitagliano, L., Verde, C., and di Prisco, G. 2006a. Minimal structural requirements for Root effect: crystal structure of the cathodic hemoglobin isolated from the Antarctic fish Trematomus newnesi. Proteins 62:316–321.

    Article  PubMed  CAS  Google Scholar 

  • Mazzarella, L., Vergara, A., Vitagliano, L., Merlino, A., Bonomi, G., Scala, S., Verde, C., and di Prisco, G. 2006b. High-resolution crystal structure of deoxy haemoglobin from Trematomus bernacchii at different pH values: the role of histidine residues in modulating the strength of the Root effect. Proteins 65:490–498.

    Article  PubMed  CAS  Google Scholar 

  • Monod, J., Wyman, J., and Changeux, J. P. 1965. On the nature of allosteric transitions: a plausible model. J. Mol. Biol. 12:88–118.

    Article  PubMed  CAS  Google Scholar 

  • Mylvaganam, S. E., Bonaventura, C., Bonaventura, J., and Getzoff, E. D. 1996. Structural basis for the Root effect in haemoglobin. Nature Struct. Biol. 3:275–283.

    Article  PubMed  CAS  Google Scholar 

  • Near, T. J., Pesavento, J. J., and Cheng, C.-H. C. 2004. Phylogenetic investigations of Antarctic notothenioid fishes (Perciformes: Notothenioidei) using complete gene sequences of the mitochondrial encoded 16S rRNA. Mol. Phylogenet. Evol. 32:881–891.

    Article  PubMed  CAS  Google Scholar 

  • Noble, R. W., Kwiatkowski, L. D., De Young, A., Davis, B. J., Haedrich, R. L., Tarn, L.T., and Riggs, A. F. 1986. Functional properties of hemoglobins from deep-sea fish: correlations with depth distribution and presence of a swimbladder. Biochim. Biophys. Acta 870:552–563.

    PubMed  CAS  Google Scholar 

  • Pelster, B. 1997. Buoyancy at depth. In Deep-Sea Fish, eds. D. Randall and A. P. Farrell, pp. 195–237. San Diego: Academic Press.

    Chapter  Google Scholar 

  • Perutz, M. F., and Brunori, M. 1982. Stereochemistry of cooperative effects in fish and amphibian hemoglobins. Nature 229:421–442.

    Article  Google Scholar 

  • Perutz, M. F., Fermi, G., Luisi, B., Shanan, B., and Liddington, R. C. 1987. Stereochemistry of cooperative mechanisms in hemoglobin. Acc. Chem. Res. 20:309–321.

    Article  CAS  Google Scholar 

  • Riggs, A. 1988. The Bohr effect. Annu. Rev. Physiol. 50:181–204.

    Article  PubMed  CAS  Google Scholar 

  • Ruud, J. T. 1954. Vertebrates without erythrocytes and blood pigment. Nature 173:848–850.

    Article  PubMed  CAS  Google Scholar 

  • Sanchez, S., Dettai, A., Bonillo, C., Ozouf-Costaz, C., Detrich, H. W. III., and Lecointre, G. 2007. Molecular and morphological phylogenies of Antarctic teleostean family Nototheniidae, with emphasis on the Trematominae. Polar Biol. 30:155–166.

    Article  Google Scholar 

  • Stam, W. T, Beintema, J. J., D’Avino, R., Tamburrini, M., and di Prisco, G. 1997. Molecular evolution of hemoglobins of Antarctic fishes (Notothenioidei). J. Mol. Evol. 45:437–445.

    Article  PubMed  CAS  Google Scholar 

  • Verde, C., De Rosa, M. C., Giordano, D., Mosca, D., de Pascale, D., Raiola, L., Cocca, E., Carratore, V., Giardina, B., and di Prisco, G. 2005. Structure, function and molecular adaptations of haemoglobins of the polar cartilaginous fish Bathyraja eatonii and Raja hyperborea. Biochem. J. 389:297–306.

    Article  PubMed  CAS  Google Scholar 

  • Verde, C., Vergara, A., Giordano, D., Mazzarella, L., and di Prisco, G. 2007. The Root effect — a structural and evolutionary perspective. Antarctic Sci 19:271–278.

    Article  Google Scholar 

  • Wittenberg, J. B., Schwend, M. J., and Wittenberg B. A. 1964. The secretion of oxygen into the swim-bladder of fish III. The role of carbon dioxide. J. Gen. Physiol. 48:337–355.

    Article  PubMed  CAS  Google Scholar 

  • Wittenberg, B. A., Briehl, R. W., and Wittenberg, J. B. 1965. Haemoglobins of invertebrate tissues. Nerve haemoglobins of Aphrodite, Aplysia and Halosydna. Biochem. J. 96:363–371.

    PubMed  CAS  Google Scholar 

  • Wittenberg, B. A., Brunori, M., Antonini, E., Wittenberg, J. B., and Wyman, J. 1965. Kinetics of the reactions of Aplysia myoglobin with oxygen and carbon monoxide. Arch. Biochem. Biophys. 111:576–579.

    Article  PubMed  CAS  Google Scholar 

  • Wittenberg, J. B., and Haedrich, R. L. 1974. The choroid rete mirabile of the fish eye. II. Distribution and relation to the pseudobranch and to the swim-bladder rete mirabile. Biol. Bull. 146:137–156.

    Article  PubMed  CAS  Google Scholar 

  • Wittenberg, J. B., and Wittenberg B. A. 1961. The secretion of oxygen into the swim-bladder of fish. II. The transport of molecular oxygen. J. Gen. Physiol. 44:527–542.

    Article  PubMed  CAS  Google Scholar 

  • Wujcik, J. M., Wang, G., Eastman, J. T., and Sidell, B. D. 2007. Morphometry of retinal vasculature in Antarctic fishes is dependent upon the level of hemoglobin in circulation. J. Exp. Biol. 210:815–824.

    Article  PubMed  CAS  Google Scholar 

  • Yokoyama, T., Chong, K. T., Miyazaki, G., Morimoto, H., Shih, D. T. B., Unzai, S., Tame, J. R. H., and Park S.-Y. 2004. Novel mechanisms of pH sensitivity in tuna hemoglobin: a structural explanation of the Root effect. J. Biol. Chem. 279:28632–28640.

    Article  PubMed  CAS  Google Scholar 

  • Yonetani, T., Park, S., Tsuneshige, A., Imai, K., and Kanaori, K. 2002. Global allostery model of hemoglobin. J. Biol. Chem. 277:34508–34520.

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2008 Springer-Verlag Italia

About this chapter

Cite this chapter

Verde, C., Berenbrink, M., di Prisco, G. (2008). Evolutionary Physiology of Oxygen Secretion in the Eye of Fishes of the Suborder Notothenioidei . In: Bolognesi, M., di Prisco, G., Verde, C. (eds) Dioxygen Binding and Sensing Proteins. Protein Reviews, vol 9. Springer, Milano. https://doi.org/10.1007/978-88-470-0807-6_7

Download citation

Publish with us

Policies and ethics