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.
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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.
Berenbrink, M. 2006. Evolution of vertebrate haemoglobins: Histidine side chains, specific buffer value and Bohr effect. Respir. Physiol. Neurobiol. 154:165–184.
Berenbrink, M. 2007. Historical reconstructions of evolving physiological complexity: O2 secretion in the eye and swimbladder of fishes. J. Exp. Biol. 209:1641–1652.
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.
Bonaventura, J., Gillen, R. G., and Riggs, A. 1974. The hemoglobin of the Crosspterygian fish, Latimeria chalumnae (Smith). Arch. Biochem. Biophys. 163:728–734.
Brittain, T. 2005. Root effect hemoglobins. J. Inorg. Biochem. 99:120–129.
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.
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.
Dettaï, A., and Lecointre, G. 2004. In search for Notothenioid (Teleostei) relatives. Antarctic Sci. 16:71–85.
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.
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.
Eastman, J. T. 2006. Aspects of the morphology of phyletically basal bovichtid fishes of the Antarctic suborder Notothenioidei (Perciformes). Polar Biol. 29:754–763.
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.
Egginton, S. 1997. A comparison of the response to induced exercise in red-and white-blooded Antarctic fishes. J. Comp. Physiol. 167:129–134.
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.
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.
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.
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.
Maddison, D. R., Maddison, W. P. 2003. MacClade 4: Analysis of phylogeny and character evolution. Version 4.06. Sinauer Associates, Sunderland, MA.
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.
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.
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.
Monod, J., Wyman, J., and Changeux, J. P. 1965. On the nature of allosteric transitions: a plausible model. J. Mol. Biol. 12:88–118.
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.
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.
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.
Pelster, B. 1997. Buoyancy at depth. In Deep-Sea Fish, eds. D. Randall and A. P. Farrell, pp. 195–237. San Diego: Academic Press.
Perutz, M. F., and Brunori, M. 1982. Stereochemistry of cooperative effects in fish and amphibian hemoglobins. Nature 229:421–442.
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.
Riggs, A. 1988. The Bohr effect. Annu. Rev. Physiol. 50:181–204.
Ruud, J. T. 1954. Vertebrates without erythrocytes and blood pigment. Nature 173:848–850.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
Yonetani, T., Park, S., Tsuneshige, A., Imai, K., and Kanaori, K. 2002. Global allostery model of hemoglobin. J. Biol. Chem. 277:34508–34520.
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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
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DOI: https://doi.org/10.1007/978-88-470-0807-6_7
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