Myoglobin oxygen affinity in aquatic and terrestrial birds and mammals

Abstract

Myoglobin (Mb) is an oxygen binding protein found in vertebrate skeletal muscle, where it facilitates intracellular transport and storage of oxygen. This protein has evolved to suit unique physiological needs in the muscle of diving vertebrates that express Mb at much greater concentrations than their terrestrial counterparts. In this study, we characterized Mb oxygen affinity (P 50 ) from 25 species of aquatic and terrestrial birds and mammals. Among diving species, we tested for correlations between Mb P 50 and routine dive duration. Across all species examined, Mb P 50 ranged from 2.40 to 4.85 mmHg. The mean P 50 of Mb from terrestrial ungulates was 3.72±0.15 mmHg (range 3.70-3.74 mmHg). The P 50 of cetaceans was similar to terrestrial ungulates ranging from 3.54 to 3.82 mmHg, with the exception of the melonheaded whale, which had a significantly higher P 50 of 4.85 mmHg. Among pinnipeds, the P 50 ranged from 3.23 to 3.81 mmHg and showed a trend for higher oxygen affinity in species with longer dive durations. Among diving birds, the P 50 ranged from 2.40 to 3.36 mmHg and also showed a trend of higher affinities in species with longer dive durations. In pinnipeds and birds, low Mb P 50 was associated with species whose muscles are metabolically active under hypoxic conditions associated with aerobic dives. Given the broad range of potential globin oxygen affinities, Mb P 50 from diverse vertebrate species appears constrained within a relatively narrow range. High Mb oxygen affinity within this range may be adaptive for some vertebrates that make prolonged dives.

Tracing whale myoglobin evolution by resurrecting ancient proteins

“…The results, however, demonstrated that the oxygen affinity of Mb was not significantly changed during the adaptation process. The P 50 values for extant animals were reported previously, and indicated that deep-sea and land animal Mbs had similar O 2 -binding affinities 49 , which was consistent with the present results. This seems to be reasonable because whales adsorb O 2 from the air on the sea surface, where p O 2 condition is similar to that for land animals, and enhancement of the O 2 affinity is not beneficial for the deep-sea adaptation.…”

Mitochondrial physiology in the skeletal and cardiac muscles is altered in torrent ducks, Merganetta armata, from high altitudes in the Andes

“…High Mb content is known to increase oxygen-storage capacity and may also promote intracellular oxygen transport (Wittenberg and Wittenberg, 2006;Koch and Britton, 2008;Mirceta et al, 2013). Diving animals rely heavily on Mb O 2 stores, rather than capillaries, for mitochondrial O 2 supply during dives, and dive duration is positively correlated with Mb concentration (Reed et al, 1994;Butler and Jones, 1997;Kooyman and Ponganis, 1998;Dolar et al, 1999;Helbo and Fago, 2012;Mirceta et al, 2013;Wright and Davis, 2015). Torrent ducks have nearly four times the Mb content reported for nonaquatic birds (Pages and Planas, 1983;Butler and Jones, 1997;Kooyman and Ponganis, 1998;Wright and Davis, 2015), suggesting that they may also have a strong dive capacity.…”

Myoglobin maturation is driven by the hsp90 chaperone machinery and by soluble guanylyl cyclase

“…The hemeprotein myoglobin (Mb) is expressed in the muscle tissue of vertebrates (1)(2)(3)(4), where it functions to store oxygen (2)(3)(4)(5)(6)(7)(8). A high level of muscle Mb expression allows certain mammals to hold their breath for longer time periods, as occurs in diving mammals like whales, seals, or dolphins (9)(10)(11)(12). Genetic depletion of Mb in mice induces several compensatory mechanisms that partly overcome its loss and thus leads to viable and fertile mice (13).…”