Functional properties of myoglobins from five whale species with different diving capacities

Abstract

SUMMARYWhales show an exceptionally wide range of diving capabilities and many express high amounts of the O 2 carrier protein myoglobin (Mb) in their muscle tissues, which increases their aerobic diving capacity. Although previous studies have mainly focused on the muscle Mb concentration and O 2 carrying capacity as markers of diving behavior in whales, it still remains unexplored whether whale Mbs differ in their O 2 affinities and nitrite reductase and peroxidase enzymatic activities, all functions that could contribute to differences in diving capacities. In this study, we have measured the functional properties of purified Mbs from five toothed whales and two baleen whales and have examined their correlation with average dive duration. Results showed that some variation in functional properties exists among whale Mbs, with toothed whale Mbs having higher O 2 affinities and nitrite reductase activities (similar to those of horse Mb) compared with baleen whale Mbs. However, these differences did not correlate with average dive duration. Instead, a significant correlation was found between whale Mb concentration and average duration and depth of dives, and between O 2 affinity and nitrite reductase activity when including horse Mb. Despite the fact that the functional properties showed little species-specific differences in vitro, they may still contribute to enhancing diving capacity as a result of the increased muscle Mb concentration found in extreme divers. In conclusion, Mb concentration rather than specific functional reactivities may support whale diving performance.

Myoglobin oxygen affinity in aquatic and terrestrial birds and mammals

“…Given the broad range of oxygen affinities that are possible by even single amino acid substitutions, Mb oxygen affinity of vertebrates is conserved within a narrow range to maintain optimal muscle performance. With the exception of the melon-headed whale, the Mb P 50 of the species in this study fell within the range previously reported for birds and mammals (Weber et al, 1974;Nichols and Weber, 1989;Helbo and Fago, 2012).…”

“…Diving species have an array of multilevel adaptations to cope with recurrent breath-holding and the subsequent hypoxia and muscular ischemia (Davis, 2014). Elevated concentrations of respiratory pigments have obvious adaptive advantages for maintaining aerobic metabolism in diving birds and mammals, and recent studies have examined the potential adaptive molecular evolution of the functional properties of these pigments Soegaard et al, 2012;Helbo and Fago, 2012;Schneuer et al, 2012;Mirceta et al, 2013). Oxygen binding globin proteins are obvious candidates for molecular adaptation in diving animals that experience regular hypoxia (Nery et al, 2013a) and Mb has experienced an increased rate of evolution in cetaceans (Nery et al, 2013b).…”

“…Among species of diving birds and mammals, Mb concentration is positively correlated with increased routine dive duration (Reed et al, 1994;Butler and Jones, 1997;Kooyman and Ponganis, 1998;Dolar et al, 1999;Helbo and Fago, 2012). In addition, Mb concentrations can vary within the musculature of an individual, with the highest concentrations found in muscles associated with routine exertion and aerobic metabolism (Polasek and Davis, 2001).…”

“…Although the structure, concentration and functional role of Mb are known to vary among birds and mammals, few studies (Nichols and Weber, 1989;Marcinek et al, 2001;Helbo and Fago, 2012) have examined the interspecfic differences in oxygen affinity using identical experimental methods. A range of Mb oxygen affinities have been reported in the literature; however, past studies used a variety of experimental techniques, instrumentation and temperatures, making comparative analysis among studies difficult.…”

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.…”