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Adaptations to Variations in Oxygen Tension by Vertebrates and Invertebrates

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Abstract

The sections in this article are:

1 Variations in Gas Tensions: Air and Water
2 Oxygen and Life
3 Respiratory Adaptations: Air Breathers
3.1 High Altitude
3.2 Borrowers
3.3 Breath‐Hold Divers
4 Water Breathers
4.1 Gas Tensions
4.2 Open Ocean
4.3 Intertidal and fresh Waters
5 Anoxic Survival
5.1 Anoxic Brain Death
5.2 Anoxic Brain Survival
6 Biochemical Adaptations
6.1 Types of Oxygen Limitation
6.2 Patterns of Metabolic Responses to Reduced Oxygen Availability
6.3 Anaerobic ATP Production
6.4 Metabolic Arrest
Figure 1. Figure 1.

Anoxic survival time of vertebrates at different temperatures. Two discrete groups are seen, one showing a more than 100‐fold capacity to survive anoxia than the other (from ref. 195).

Figure 2. Figure 2.

Metabolic responses to oxygen lack by mouse and turtle brain. Time‐dependent changes in ATP (circles), creatine phosphate (triangles), and lactate (squares) are shown. ATP levels are rapidly depleted in mouse brain. Turtle brain shows a significant drop in ATP during the hypoxic transition period (10 min), and this is reversed when metabolic arrest mechanisms are applied in anoxia (data from refs. 173,193).

Figure 3. Figure 3.

Role of neurotransmitters in anoxic survival of turtle brain. Soon after the turtle brain is exposed to anoxia there is a fall in ATP, which may serve as an early signal of energy insufficiency. Degradation of ATP leads to an increase in adenosine, which is released to the extracellular space. Adenosine causes a decrease in ATP use by inhibiting neuronal excitability and effects an increase in substrate (that is, glucose) supply by increasing cerebral blood flow. ATP levels are consequently restored. A sustained release of inhibitory amino acids follows, which consolidates the hypometabolic state of the anoxic brain by further decreasing its activity and energy demands (redrawn from ref. 194).

Figure 4. Figure 4.

Phosphagens and imino acid end‐products in animals.

Figure 5. Figure 5.

Schematic diagram showing the relationships between oxygen availability, ATP demand by cellular metabolism, and ATP output from oxidative and fermentative pathways for hypoxia/anoxia‐intolerant species vs. facultative anaerobes. Stippled area shows the shortfall in ATP output compared with ATP demand that leads to metabolic failure at low oxygen tensions in hypoxia/anoxia‐intolerant species. By contrast, facultative anearobes sharply suppress ATP demand when oxygen availability is restricted to a level that can be met by the output of fermentative pathways alone.

Figure 6. Figure 6.

Pathway of ethanol production as an anaerobic end‐product in goldfish skeletal muscle. PDC, pyruvate dehydrogenase complex; ADH, alcohol dehydrogenase.

Figure 7. Figure 7.

Pathways of anaerobic energy production in marine invertebrates. A: In early anoxia, the catabolism of glycogen to alanine is coupled with the conversion of aspartate to succinate. B: Later in anoxia, glycolytic carbon is fed, via phosphoenolpyruvate carboxykinase, directly into the synthesis of succinate, acetate, and proprionate. Malate dismutation in the mitochondria results in a 1:2 synthesis of acetate:proprionate that maintains redox balance at the fumarate reductase reaction. C: Phospoenolpyruvate and pyruvate branchpoints direct glycolytic carbon flow to different end‐products under different metabolic circumstances. PEP, phosphoenolpyruvate; PYR, pyruvate; OXA, oxaloacetate; MAL, malate; FUM, fumarate; ACoA, acetyl‐coenzyme A; MM‐CoA, methylmalonyl‐coenzyme A.

Figure 8. Figure 8.

Typical pattern of substrate utilization and end‐product accumulation over the course of anoxic exposure in marine molluscs. Volatile fatty acids are excreted into external seawater.

Figure 9. Figure 9.

Coordinated suppression of F2, 6P2 levels and the activities of glycogen phosphorylase, phosphofructokinases 1 and 2 (PFK‐1, PFK‐2), and pyruvate kinase (PK) in whelk gill over 20 h exposure to N20 bubbled seawater (from ref. 277).



Figure 1.

Anoxic survival time of vertebrates at different temperatures. Two discrete groups are seen, one showing a more than 100‐fold capacity to survive anoxia than the other (from ref. 195).



Figure 2.

Metabolic responses to oxygen lack by mouse and turtle brain. Time‐dependent changes in ATP (circles), creatine phosphate (triangles), and lactate (squares) are shown. ATP levels are rapidly depleted in mouse brain. Turtle brain shows a significant drop in ATP during the hypoxic transition period (10 min), and this is reversed when metabolic arrest mechanisms are applied in anoxia (data from refs. 173,193).



Figure 3.

Role of neurotransmitters in anoxic survival of turtle brain. Soon after the turtle brain is exposed to anoxia there is a fall in ATP, which may serve as an early signal of energy insufficiency. Degradation of ATP leads to an increase in adenosine, which is released to the extracellular space. Adenosine causes a decrease in ATP use by inhibiting neuronal excitability and effects an increase in substrate (that is, glucose) supply by increasing cerebral blood flow. ATP levels are consequently restored. A sustained release of inhibitory amino acids follows, which consolidates the hypometabolic state of the anoxic brain by further decreasing its activity and energy demands (redrawn from ref. 194).



Figure 4.

Phosphagens and imino acid end‐products in animals.



Figure 5.

Schematic diagram showing the relationships between oxygen availability, ATP demand by cellular metabolism, and ATP output from oxidative and fermentative pathways for hypoxia/anoxia‐intolerant species vs. facultative anaerobes. Stippled area shows the shortfall in ATP output compared with ATP demand that leads to metabolic failure at low oxygen tensions in hypoxia/anoxia‐intolerant species. By contrast, facultative anearobes sharply suppress ATP demand when oxygen availability is restricted to a level that can be met by the output of fermentative pathways alone.



Figure 6.

Pathway of ethanol production as an anaerobic end‐product in goldfish skeletal muscle. PDC, pyruvate dehydrogenase complex; ADH, alcohol dehydrogenase.



Figure 7.

Pathways of anaerobic energy production in marine invertebrates. A: In early anoxia, the catabolism of glycogen to alanine is coupled with the conversion of aspartate to succinate. B: Later in anoxia, glycolytic carbon is fed, via phosphoenolpyruvate carboxykinase, directly into the synthesis of succinate, acetate, and proprionate. Malate dismutation in the mitochondria results in a 1:2 synthesis of acetate:proprionate that maintains redox balance at the fumarate reductase reaction. C: Phospoenolpyruvate and pyruvate branchpoints direct glycolytic carbon flow to different end‐products under different metabolic circumstances. PEP, phosphoenolpyruvate; PYR, pyruvate; OXA, oxaloacetate; MAL, malate; FUM, fumarate; ACoA, acetyl‐coenzyme A; MM‐CoA, methylmalonyl‐coenzyme A.



Figure 8.

Typical pattern of substrate utilization and end‐product accumulation over the course of anoxic exposure in marine molluscs. Volatile fatty acids are excreted into external seawater.



Figure 9.

Coordinated suppression of F2, 6P2 levels and the activities of glycogen phosphorylase, phosphofructokinases 1 and 2 (PFK‐1, PFK‐2), and pyruvate kinase (PK) in whelk gill over 20 h exposure to N20 bubbled seawater (from ref. 277).

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Peter L. Lutz, Kenneth B. Storey. Adaptations to Variations in Oxygen Tension by Vertebrates and Invertebrates. Compr Physiol 2011, Supplement 30: Handbook of Physiology, Comparative Physiology: 1479-1522. First published in print 1997. doi: 10.1002/cphy.cp130221