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Open Access Highly Accessed Research article

Molecular basis of a novel adaptation to hypoxic-hypercapnia in a strictly fossorial mole

Kevin L Campbell1*, Jay F Storz2, Anthony V Signore1, Hideaki Moriyama2, Kenneth C Catania3, Alexander P Payson4, Joseph Bonaventura4, Jörg Stetefeld5 and Roy E Weber6

Author Affiliations

1 Department of Biological Sciences, University of Manitoba, Winnipeg, MB R3T 2N2 Canada

2 School of Biological Sciences, University of Nebraska, Lincoln, NE 68588, USA

3 Department of Biological Sciences, Vanderbilt University, Nashville, TN 37235, USA

4 Duke University Medical Center and Nicholas School of the Environment Marine Laboratory, Beaufort, NC 28516, USA

5 Department of Chemistry, University of Manitoba, Winnipeg, MB R3T 2N2 Canada

6 Zoophysiology, Institute of Biological Sciences, University of Aarhus, Aarhus, DK 8000, Denmark

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BMC Evolutionary Biology 2010, 10:214  doi:10.1186/1471-2148-10-214

Published: 16 July 2010

Abstract

Background

Elevated blood O2 affinity enhances survival at low O2 pressures, and is perhaps the best known and most broadly accepted evolutionary adjustment of terrestrial vertebrates to environmental hypoxia. This phenotype arises by increasing the intrinsic O2 affinity of the hemoglobin (Hb) molecule, by decreasing the intracellular concentration of allosteric effectors (e.g., 2,3-diphosphoglycerate; DPG), or by suppressing the sensitivity of Hb to these physiological cofactors.

Results

Here we report that strictly fossorial eastern moles (Scalopus aquaticus) have evolved a low O2 affinity, DPG-insensitive Hb - contrary to expectations for a mammalian species that is adapted to the chronic hypoxia and hypercapnia of subterranean burrow systems. Molecular modelling indicates that this functional shift is principally attributable to a single charge altering amino acid substitution in the β-type δ-globin chain (δ136Gly→Glu) of this species that perturbs electrostatic interactions between the dimer subunits via formation of an intra-chain salt-bridge with δ82Lys. However, this replacement also abolishes key binding sites for the red blood cell effectors Cl-, lactate and DPG (the latter of which is virtually absent from the red cells of this species) at δ82Lys, thereby markedly reducing competition for carbamate formation (CO2 binding) at the δ-chain N-termini.

Conclusions

We propose this Hb phenotype illustrates a novel mechanism for adaptively elevating the CO2 carrying capacity of eastern mole blood during burst tunnelling activities associated with subterranean habitation.