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Biology

Now we got bad blood: Oxygen binding is not affected by haemoglobin subtype in Atlantic cod

Barlow, S.L., J. Metcalfe, D.A. Righton, and M. Berenbrink. (2017). Life on the edge: O2 binding in Atlantic cod red blood cells near their southern distribution limit is not sensitive to temperature or haemoglobin genotype. J. Exp. Biol. 220: 414-424.

The collapse of the Atlantic northwest cod fishery is a textbook example of the consequences of overfishing [Wikimedia].

The collapse of the Atlantic northwest cod fishery is a textbook example of the consequences of overfishing [Wikimedia].

If you’ve ever had English-style fish and chips, you’ve probably tasted the dense, flaky flesh of cod. On this side of the Atlantic, these fish are perhaps most famous for the catastrophic 1992 collapse of the Grand Banks stock. While the Canadian fishery remains closed, and recovery of the population has been slow, there are recent, encouraging signs of a comeback.

Atlantic cod all over the world are expected to be hit hard by climate change, as warming ocean temperatures have already been associated with declining populations in the southern boundaries of their range in the Irish and North Seas.

Oxygen- and capacity-limited thermal tolerance

Atlantic cod (Gadus morhua) [Wikimedia]

Atlantic cod (Gadus morhua) [Wikimedia]

What happens when animals get too hot? Why is a tropical cichlid happy in a 28°C aquarium while the same temperature would stress out a goldfish? The physiology of coping with high temperatures and how global warming may impact future fish stocks is an active area of research. One of the big questions is what sets the limit of thermal tolerance in “cold-blooded” ectotherms like fish, reptiles, and amphibians.

A widely, but not universally, accepted theory is Oxygen- and Capacity-Limited Thermal Tolerance (OCLTT), which argues that failure of the cardiorespiratory system restricts the ability of animals to cope with extreme temperatures (Ern et al., 2015; Portner, 2010). When ectotherms heat up, their metabolic rate and oxygen demands increase. This puts pressure on the cardiorespiratory system to supply more oxygen to the tissues through responses like increasing ventilation rate, heart rate, or the number of oxygen-carrying red blood cells.

OCLTT contends that an animal hits its upper thermal limits when metabolic demand outruns their ability to supply oxygen to body tissues. This results in a dramatic loss in performance, and limits the thermal range of a species, shaping its ecology and habitat preferences.

The central role of haemoglobin in oxygen transport

Haemoglobin, the protein that gives red blood cells their colour, binds to oxygen when passing through the gills (or lungs) and carries this oxygen to the tissues, where it is off-loaded and taken in by cells. How effectively haemoglobin binds to oxygen (haemoglobin-O2 affinity) is key to an animal’s oxygen transport capacity. Animals that tolerate oxygen-poor conditions, like high altitude birds and mammals, often have high-affinity haemoglobin that is very good at binding to oxygen, helping them extract as much as possible from their environment.

Increasing temperature causes the rightward shift of the oxygen binding curve. This reduction in binding affinity means a greater partial pressure (i.e. more oxygen) is needed to achieve the same oxygen saturation (i.e. oxygen binding) of haemoglobin at 38 degrees compared to 20 degrees [Wikimedia].

Increasing temperature causes the rightward shift of the oxygen binding curve. This reduction in binding affinity means a greater partial pressure (i.e. more oxygen) is needed to achieve the same oxygen saturation (i.e. oxygen binding) of haemoglobin at 38 degrees compared to 20 degrees [Wikimedia].

Haemoglobin-O2 binding is extremely sensitive to conditions within the red blood cell, and this can be exploited to fine-tune circulatory oxygen transport. Increasing temperature or carbon dioxide levels (or reducing pH) will reduce haemoglobin-O2 affinity because it promotes off-loading (“de-binding”) of oxygen from haemoglobin. High performance animals with high metabolic rates, like tuna or mice, may have haemoglobin that is very sensitive to high temperatures or low pH (two conditions that develop in exercising muscles) to encourage their red blood cells to dump as much oxygen as possible they pass oxygen-hungry tissues.

Atlantic cod haemoglobin polymorphism

The fish used in this study were caught in the Barents Sea, in the far north, and from the (ironically southern) North Sea population [Wikimedia].

The fish used in this study were caught in the Barents Sea, in the far north, and from the (ironically southern) North Sea population [Wikimedia].

Atlantic cod possess two haemoglobin gene variants (alleles), HbI 1 and HbI 2, and three haemoglobin subtypes (HbI 1/1, HbI 1/2, and HbI 2/2) based upon the combination of alleles that a fish inherited from its parents. Haemoglobin subtypes in cod are somewhat analogous to the ABO system of human blood typing, where AB (like HbI 1/2) is a distinct blood type because the A and B alleles are co-dominant (otherwise a person with AB alleles would present as type A or type B only).

Interestingly, the frequency of the haemoglobin variants follows a geographical distribution – the HbI 1 allele occurs in less than 10% of the northern Barents Sea population, and becomes increasing common in more southern cod populations, occurring in 60 to 70% of fish living in the southern North Sea. In addition to geographical distribution, haemoglobin subtypes have been associated with variation in growth rates, preferred temperatures, and tolerance to low-oxygen conditions.

Connecting the dots

Fetal haemoglobin has higher affinity than adult haemoglobin, and this helps ensure oxygen moves from the mother's blood into her baby's blood. Perhaps HbI 1/1, HbI 1/2, and Hb 2/2 had similar differences in affinity? [Wikimedia]

Fetal haemoglobin has higher affinity than adult haemoglobin, and this helps ensure oxygen moves from the mother’s blood into her baby’s blood. Perhaps HbI 1/1, HbI 1/2, and Hb 2/2 had similar differences in affinity? [Wikimedia]

While researchers have known since the 1960’s that different haemoglobin alleles exist in Atlantic cod, and that they vary down a latitudinal (and temperature) gradient, no one has ever experimentally verified the link between cod haemoglobin subtype and thermal sensitivity. Seeing this gap in the scientific literature, Barlow and colleagues recently compared the oxygen binding ability of cod haemoglobins under different environmental conditions. Are HbI 1/1, HbI 1/2, and HbI 2/2 haemoglobins functionally different? Did the southern HbI 1 allele respond differently to higher temperatures, perhaps leading to greater oxygen transport capacity and performance in the warmer waters?

Haemoglobin subtype doesn’t matter

A single haemoglobin molecule can carry up to four molecules of oxygen [Wikimedia].

A single haemoglobin molecule can carry up to four molecules of oxygen [Wikimedia].

Sometimes research projects yield more questions than answers.

Unexpectedly, an individual’s haemoglobin subtype had no effect on its O2-binding properties – HbI 1/1, HbI 1/2, and HbI 2/2 proteins were indistinguishable regardless of experimental pH or temperature. Perhaps the potential adaptive value of different haemoglobin subtypes for oxygen transport had been overemphasized in previous studies.

Atlantic cod are benthopelagic, meaning they like to sit near the bottom [Flickr]

Atlantic cod are benthopelagic, meaning they like to sit near the bottom [Flickr]

Alternatively, haemoglobin subtypes may be linked to other, more subtle characteristics that are more advantageous in certain environments, leading to differences in allele frequency. For example, unfertilized cod eggs have transcripts (“biological blueprints” to build a protein) for all adult globins, but these disappear soon after the egg is fertilized during spawning. Maybe these transcripts have some role in fertilization rate, leading to embryos with HbI 1 alleles to be more successful in southern waters.

Clearly, the story is messier than we thought, emphasizing the importance of “fact-checking” even well-reasoned assumptions. As ocean temperatures continue to rise, further work is needed to uncover the links between physiology, ecology, and evolution so we can better understand and predict how animals will respond to climate change.

 

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