Oxygenation properties and isoform diversity of snake hemoglobins

Authors

Jay F. Storz, University of Nebraska-LincolnFollow
Chandrasekhar Natarajan, University of Nebraska-LincolnFollow
Hideaki Moriyama, University of Nebraska-LincolnFollow
Federico G. Hoffmann, Mississippi State UniversityFollow
Tobias Wang, Aarhus UniversityFollow
Angela Fago, Aarhus University, DenmarkFollow
Hans Malte, Aarhus UniversityFollow
Johannes Overgaard, Aarhus UniversityFollow
Roy E. Weber, Aarhus University, DenmarkFollow

Date of this Version

2015

Citation

Published in American Journal of Physiology — Regulatory, Integrative and Comparative Physiology vol. 309, no. 9 (1 November 2015), pp. R1178–R1191; doi: 10.1152/ajpregu.00327.2015 ; PubMed PMID 26354849

Comments

Copyright © 2015 American Physiological Society. Used by permission.

Abstract

Available data suggest that snake hemoglobins (Hbs) are characterized by a combination of unusual structural and functional properties relative to the Hbs of other amniote vertebrates, including oxygenation-linked tetramer-dimer dissociation. However, standardized comparative data are lacking for snake Hbs, and the Hb isoform composition of snake red blood cells has not been systematically characterized. Here we present the results of an integrated analysis of snake Hbs and the underlying α- and β-type globin genes to characterize 1) Hb isoform composition of definitive erythrocytes, and 2) the oxygenation properties of isolated isoforms as well as composite hemolysates. We used species from three families as subjects for experimental studies of Hb function: South American rattlesnake, Crotalus durissus (Viperidae); Indian python, Python molurus (Pythonidae); and yellow- bellied sea snake, Pelamis platura (Elapidae). We analyzed allosteric properties of snake Hbs in terms of the Monod-Wyman-Changeux model and Adair four-step thermodynamic model. Hbs from each of the three species exhibited high intrinsic O₂ affinities, low cooperativities, small Bohr factors in the absence of phosphates, and high sensitivities to ATP. Oxygenation properties of the snake Hbs could be explained entirely by allosteric transitions in the quaternary structure of intact tetramers, suggesting that ligation-dependent dissociation of Hb tetramers into αβ-dimers is not a universal feature of snake Hbs. Surprisingly, the major Hb isoform of the South American rattlesnake is homologous to the minor HbD of other amniotes and, contrary to the pattern of Hb isoform differentiation in birds and turtles, exhibits a lower O₂ affinity than the HbA isoform.