High-affinity hemoglobin and blood oxygen saturation in diving emperor penguins

Abstract

SUMMARYThe emperor penguin (Aptenodytes forsteri) thrives in the Antarctic underwater environment, diving to depths greater than 500 m and for durations longer than 23 min. To examine mechanisms underlying the exceptional diving ability of this species and further describe blood oxygen (O 2 ) transport and depletion while diving, we characterized the O 2 -hemoglobin (Hb) dissociation curve of the emperor penguin in whole blood. This allowed us to (1) investigate the biochemical adaptation of Hb in this species, and (2) address blood O 2 depletion during diving, by applying the dissociation curve to previously collected partial pressure of O 2 (P O2 ) profiles to estimate in vivo Hb saturation (S O2 ) changes during dives. This investigation revealed enhanced Hb-O 2 affinity (P 50 =28 mmHg, pH 7.5) in the emperor penguin, similar to high-altitude birds and other penguin species. This allows for increased O 2 at low blood P O2 levels during diving and more complete depletion of the respiratory O 2 store. S O2 profiles during diving demonstrated that arterial S O2 levels are maintained near 100% throughout much of the dive, not decreasing significantly until the final ascent phase. End-of-dive venous S O2 values were widely distributed and optimization of the venous blood O 2 store resulted from arterialization and near complete depletion of venous blood O 2 during longer dives. The estimated contribution of the blood O 2 store to diving metabolic rate was low and highly variable. This pattern is due, in part, to the influx of O 2 from the lungs into the blood during diving, and variable rates of tissue O 2 uptake.

Neuroglobin of seals and whales: Evidence for a divergent role in the diving brain

“…Qvist et al, 1986;Meir and Ponganis, 2009). Many physiological adaptations of whales and seals have been reported, but little is still known about how their brains copes with the challenges of the hypoxic environment and which molecular mechanisms are involved.…”

“…In contrast to most terrestrial mammals, diving mammals (i.e. whales and seals) are routinely exposed to severe hypoxia when submerged (Qvist et al, 1986;Meir and Ponganis, 2009); however, they survive these critical conditions without any obvious damage and even show remarkable diving capacities during foraging. So far, many physiological adaptations optimizing oxygen supply and metabolic demands in relevant tissues of diving mammals have been reported (for review, see: Butler and Jones, 1997;Butler, 2004;Ramirez et al, 2007).…”

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

“…It is possible that hypoxia exposure associated with breath-holding diving led to exaptations ( pre-adaptations) for life at high altitudes in lowland torrent ducks, and reduced the selective advantage for adaptive changes in some traits in the high-altitude population. Consistent with this idea, both high-and low-altitude populations of torrent ducks have hemoglobin with an affinity (P 50 =33-35 mmHg) that is much greater than most birds (in which P 50 typically ranges between 44 and 52 mmHg) and is comparable to that of the emperor penguin (P 50 =28-36 mmHg) (Christensen and Dill, 1935;Hirsowitz et al, 1977;Lutz, 1980;Wastl and Leiner, 1931;Meir and Ponganis, 2009;Tamburrini et al, 1994;Natarajan et al, 2015). However, unlike highland populations of many other South American waterfowl, highland torrent ducks lack further evolved specialization in hemoglobin sequence or O 2 -binding affinity compared to their lowland counterparts (McCracken et al, 2009a,b).…”

The oxidative debt of fasting: evidence for short to medium-term costs of advanced fasting in adult king penguins

“…Interestingly, one common life-history feature of penguins and seals is the alternation of long deepdiving events with short surface events for breathing. These animals have to cope with prolonged apnoea, exposing tissues to high levels of hypoxemia due to high pressure when diving, followed by rapid tissue re-perfusion and transiently high oxygen concentration in tissues during brief surface episodes (Meir and Ponganis, 2009). This situation, known as ischemia-reperfusion, induces the mass activation of nitric oxide synthase (Huang et al, 1994;Iadecola et al, 1997) and xanthine oxidase (Granger, 1988), enzymes known to promote ROS.…”

“…Indeed, in addition to high metabolic rates that may result in the by-production of large quantities of ROS (Beckman and Ames, 1998;Stier et al, 2014a,b; but see Speakman and Selman, 2011), king penguins forage in apnoea during repetitive diving bouts (>1000 foraging dives per trip; Bost et al, 2007) carried out at high ambient pressure (>100 m diving depth; Kooyman et al, 1992). This temporarily exposes their tissues to critically low levels of oxygen (hypoxemia), before the transient re-perfusion of oxygen-rich blood when reaching the surface again -a situation known as ischemiareperfusion (Meir and Ponganis, 2009), which may cause massive bursts of oxidative stress (Chouchani et al, 2016). Whereas deepdiving animals have typically evolved efficient antioxidant defences to deal with such a situation (Vázquez-Medina et al, 2011, 2012Zenteno-Savin et al, 2010), penguins at an advanced stage of energy depletion may have compromised defence mechanisms, making it harder to cope with oxidative stress.…”