Proceedings of The Physiological Society
University of Birmingham (2010) Proc Physiol Soc 20, C07
Cardiac adaptations to hypoxia in the high-altitude bar-headed goose
G. R. Scott1,2, P. M. Schulte2, S. Egginton3, A. L. Scott2, J. G. Richards2, W. K. Milsom2
1. School of Biology, University of St Andrews, St Andrews, United Kingdom. 2. Department of Zoology, University of British Columbia, Vancouver, British Columbia, Canada. 3. Angiogenesis Research Group, Centre for Cardiovascular Sciences, University of Birmingham Medical School, Birmingham, United Kingdom.
Bar-headed geese fly at up to 9000m elevation during their migration over the Himalayas, sustaining high metabolic rates in the severe hypoxia at these altitudes. Previous work suggests that adaptations to enhance pulmonary O2 loading and peripheral O2 diffusion exist in bar-headed geese [1,2], but very little is otherwise known about the mechanisms for this physiological feat. We used a comparative approach to investigate whether specializations in cardiac O2 transport and energy metabolism contribute to hypoxia adaptation in this species. Bar-headed geese had higher capillary densities in the left ventricle of the heart than low-altitude geese (bar-headed geese: 2795 ± 125 mm-2, N=6; pink-footed geese: 2070 ± 38, N=8; barnacle geese: 2228 ± 109, N=8; significance tested with ANOVA and Holm-Sidak post-hoc tests), which should improve O2 diffusion during hypoxia. While myoglobin abundance and the activities of many metabolic enzymes showed only minor variation between species, bar-headed geese had a striking alteration in the kinetics of cytochrome c oxidase (COX), the heteromeric enzyme that catalyzes O2 reduction in oxidative phosphorylation. This was reflected by a lower maximum catalytic activity (Vmax; bar-headed geese: 2.04 ± 0.24 µmol/mg protein/min; pink-footed geese: 3.85 ± 0.36; barnacle geese: 4.37 ± 0.38) and a higher affinity for reduced cytochrome c (Km; bar-headed geese: 39.8 ± 7.7 µmol; pink-footed geese: 179.8 ± 28.6; barnacle geese: 179.1 ± 18.1). There were small differences between species in mRNA and protein expression of COX subunits 3 and 4, but these were inconsistent with the divergence in enzyme kinetics. However, the COX3 gene of bar-headed geese had an amino acid substitution at a site that is otherwise conserved across vertebrates and resulted in a major functional change of amino acid class (Trp-116→Arg; the former was present in all 606 vertebrate species available in Genbank). This mutation was predicted by structural modelling to alter the interaction between COX3 and COX1. Adaptations in mitochondrial enzyme kinetics and O2 transport capacity may therefore contribute to the exceptional ability of bar-headed geese to fly high.
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