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

Kevin L. Campbell, Jay F. Storz, Anthony V. Signore, Hideaki Moriyama, Kenneth C. Catania, Alexander P. Payson, Joseph Bonaventura, Jörg Stetefeld, Roy E. Weber

Research output: Contribution to journalArticlepeer-review

37 Scopus citations

Abstract

Background. Elevated blood O2affinity enhances survival at low O2pressures, 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 O2affinity 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 O 2affinity, 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 -type -globin chain (136GlyGlu) of this species that perturbs electrostatic interactions between the dimer subunits via formation of an intra-chain salt-bridge with 82Lys. 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 82Lys, thereby markedly reducing competition for carbamate formation (CO2binding) at the -chain N-termini. Conclusions. We propose this Hb phenotype illustrates a novel mechanism for adaptively elevating the CO 2carrying capacity of eastern mole blood during burst tunnelling activities associated with subterranean habitation.

Original languageEnglish (US)
Article number214
JournalBMC Evolutionary Biology
Volume10
Issue number1
DOIs
StatePublished - 2010

ASJC Scopus subject areas

  • Ecology, Evolution, Behavior and Systematics

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