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Vascular Expression of Hemoglobin Alpha in Antarctic Icefish Supports Iron Limitation as Novel Evolutionary Driver

Bruce A. Corliss, Leon J. Delalio, T.C. Stevenson Keller IV, Alexander S. Keller, Douglas A. Keller, Bruce H. Corliss, Adam C Bjork, Jody M. Beers, Shayn M. Peirce, Brant E. Isakson

Posted on: 15 August 2019

Preprint posted on 19 July 2019

Article now published in Frontiers in Physiology at http://dx.doi.org/10.3389/fphys.2019.01389

Is the loss of hemoglobin in the Antarctic icefish a result of an extreme iron limitation adaptation?

Selected by Charlotte Nelson

Context

The Antarctic icefish (Channichthyidae) represent a unique family of species who are well known for their loss of the oxygen binding protein hemoglobin. Many species also lack myoglobin and consequently are only able to transport oxygen physically dissolved in the plasma. This apparent maladaptation is thought to be a strategy to reduce blood viscosity at the freezing temperatures the icefish experience in their Southern Ocean home (1.5 to -1.9 °C). Consequently they have developed various compensatory traits including; increased plasma volume, larger blood vessels, cardiac hypertrophy, and plasma accessible carbonic anhydrase at the gill. It has been suggested that the icefish survive what would be expected to be a catastrophic loss as a result of relaxed selection pressure; their habitat in the Southern Ocean contains few predators and the extremely stable, cold temperatures allow full saturation of oxygen in the water.

An often overlooked consequence of the loss of hemoglobin is the decrease in the need for iron. Iron is the key element involved in the hemoglobin and myoglobin binding proteins and can account for 70% of an animals total iron utilization. Additionally, it has been shown that bioavailable iron is a limiting nutrient in many aquatic ecosystems.

 

Iron limitation as an evolutionary driver for hemoglobin loss

The iron hypothesis posits that in oceanic ecosystems iron is a limiting nutrient and when added to the system is sufficient to cause large scale phytoplankton blooms. There is already evidence for iron minimization adaptations in the Southern Ocean phytoplankton that form the base of the food chain; such scarcity of iron in phytoplankton means that organisms higher on the food chain only receive a fraction of the iron compared to other environments. Therefore adaptations to minimize iron requirements throughout the food chain would enable the ecosystem to support greater biomass, and indeed the Southern Ocean appears to show such characteristics. Therefore, the current study proposes that iron limitation may be a significant driver of icefish evolution, providing the strong selective pressure required to sustain icefish species despite the loss of hemoglobin and myoglobin.

Icefishes are often considered to be an example of total hemoglobin loss via the Hb beta (Hbb) gene deletion and Hb alpha (Hba) gene truncation. However this study provides evidence for expression of the truncated Hba protein in the retinal endothelium suggesting there is some selective pressure preventing the complete loss of this gene. This partial retention of hemoglobin expression illustrates that a complete loss of hemoglobin is likely detrimental or even fatal.

 

Heightened nitric oxide availability

In addition to its role as an oxygen binding protein, the Hba protein has been shown to modulate endothelial nitric oxide flux involved in vascular remodelling at myoendothelial junctions. Hba binds to endothelial nitric oxide synthase and acts as a scavenger of nitric oxide thereby acting as a negative regulator for the availability of endothelial nitric oxide reaching smooth muscle cells. Disruption of this interaction results in smooth muscle vasodilation and blood pressure reduction. Therefore, the retention of the truncated Hba protein may indicate a role in maintaining this key process and protecting from nitric oxide toxicity. Indeed the compensatory adaptations for the loss of hemoglobin assisted oxygen transport (e.g. vasodilation, cardiac hypertrophy etc.) may be facilitated through nitric oxide signalling, and therefore potentially impossible under conditions of complete deletion of the Hba gene.

 

Open questions

  1. Is it likely that Hbais expressed homogenously in the icefish vasculature, or just in the retinal endothelium?

 

References

Beers, J.M. and Sidell, B. D. (2011). Thermal tolerance of Antarctic notothenioid fishes correlated with level of circulating hemoglobin. Physiol. Biochem. Zool. 84, 353-362.

Martin, J. H. et al., (1994). Testing the iron hypothesis in ecosystems of the equatorial pacific ocean. Nature, 371, 123-129.

Tags: antarctica, hemoglobin, icefish

doi: https://doi.org/10.1242/prelights.13321

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Author's response

Bruce A. Corliss shared

Hi Charlotte,

Thank you for highlighting our paper for The Company of Biologists, we really appreciate it!!

In response to your query in the highlight:
Although the finding awaits confirmation and we are limited to speculation, we believe that the truncated Hba protein is likely expressed in the endothelium across icefish tissues. If this is the case, an intriguing follow-up investigation is whether this Hba expression is localised to the microvasculature, or also includes the macrovasculature, and may give further insight into its function.

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