In the early 1900s, August Krogh shaped the way we think of oxygen uptake in mammalian lungs and oxygen release at the level of tissues as two processes that occur passively, from an area of high oxygen partial pressure to one of lower partial pressure until the two sides are in equilibrium. Using this mammalian model, we have assumed that these processes are identical across all vertebrate species. However, recent studies in teleost fish have challenged the assumption that the diffusion proceeds unaided, and have provided evidence that fishes, particularly those that withstand long migrations, have evolved a mechanism that increases oxygen unloading efficiency at the level of tissues: a protein called carbonic anhydrase that is located in the blood plasma.
Till Harter, from University of British Columbia, Canada, along with a group of researchers from Memorial University of Newfoundland, Canada, decided to challenge the dogma on the fate of oxygen in the fish body by demonstrating that the evolution of the plasma carbonic anhydrase allows for efficient oxygen unloading at the tissues following a swim challenge. To this end, the researchers acclimated Atlantic salmon (Salmo salar) – which perform epic migrations from their spawning grounds out to sea and back – to water containing either 95–100% oxygen air saturation (normal oxygen levels) or 40% oxygen air saturation (low oxygen) for 6–10 weeks.
The team then set both groups of fish swimming for 1.5 h in well-oxygenated water before injecting them with a chemical that blocks the activity of the blood plasma carbonic anhydrase, C18, which should reduce the ability of the fish to supply oxygen to their tissues, making the heart work harder if they were dependent on the enzyme to boost the oxygen supply to their tissues. The scientists found that the volume of blood pumped by the heart per minute (known as the cardiac output) increased immediately after the injection and was ∼27% higher, regardless of whether they were adapted to swimming in normal water or low oxygen conditions. So, having knocked out the plasma carbonic anhydrase, the fish hearts were compensating for the loss by working harder to increase oxygen delivery to the tissues. However, during the fish's recovery, the role of blood plasma carbonic anhydrase in oxygen delivery became more apparent. The hearts of the fish that had been that been living in poorly oxygenated water continued pumping harder than the hearts of the fish that been kept in fully oxygenated water as they got over the exertion, suggesting that prior acclimation to low oxygen had conditioned the fish to rely more on plasma carbonic anhydrase to increase tissue oxygen unloading efficiency.
This study is one of the first to show the significant role that plasma carbonic anhydrase plays in the tissues of migratory bony fishes. The authors have shown that, by increasing the oxygen unloading capacity at the tissues through the action of the plasma carbonic anhydrase, migrating fishes are not only able to decrease the load on their hearts by 30%, but can also employ this mechanism while exercising and during recovery. Having an effective way of getting oxygen to the tissues is an incredible adaptation, one that Atlantic salmon take full advantage of, especially during their 300 km migrations to their spawning grounds!