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

Abstract

Frigid temperatures of the Southern Ocean are known to be an evolutionary driver in Antarctic fish. For example, many fish have reduced red blood cell (RBC) concentration to minimize vascular resistance. Via the oxygen-carrying protein hemoglobin, RBCs contain the vast majority of the body’s iron, which is known to be a limiting nutrient in marine ecosystems. Since lower RBC levels also lead to reduced iron requirements, we hypothesize that low iron availability was an additional evolutionary driver of Antarctic fish speciation. Antarctic Icefish of the family Channichthyidae are known to have an extreme alteration of iron metabolism due to loss of RBCs and two iron-binding proteins, hemoglobin and myoglobin. Loss of hemoglobin is considered a maladaptive trait allowed by relaxation of predator selection since extreme adaptations are required to compensate for the loss of oxygen-carrying capacity. However, iron dependency minimization may have driven hemoglobin loss instead of a random evolutionary event. Given the variety of functions that hemoglobin serves in the endothelium, we suspected the protein corresponding to the 3’ truncated Hbα fragment (Hbα-3’f) that was not genetically excluded by icefish may still be expressed as a protein. Using whole mount confocal microscopy, we show that Hbα-3’f is expressed in the vascular endothelium of icefish retina, suggesting this Hbα fragment may still serve an important role in the endothelium. These observations support a novel hypothesis that iron minimization could have influenced icefish speciation with the loss of the iron-binding portion of Hbα in Hbα-3’f, as well as hemoglobin β and myoglobin.

Genomics of Secondarily Temperate Adaptation in the Only Non-Antarctic Icefish

“…Even after the evolution of these phenotypes, icefish still exhibit limited cardiac performance, with <10% of the oxygen carrying capacity of red-blooded notothenioids ( Holeton 1970 ) and far larger cardiac energy expenditures ( Tota et al 1991 ; Tota and Gattuso 1996 ). Given these biological limitations, the loss of hemoglobin in icefish was often considered to be maladaptive ( Sidell and O’Brien 2006 ), although recent work has proposed alternative hypotheses related to adaptive changes in the presence of sparse iron and alternative functional roles for partial hemoglobin fragments ( Corliss et al 2019 ). Regardless of the evolutionary mechanism behind the loss, the derived physiology stemming from the lack of hemoglobin is predicted to limit icefishes’ adaptive potential to migrate to warmer waters or to respond to rapidly changing ocean temperatures.…”

Genomics of Secondarily Temperate Adaptation in the Only Non-Antarctic Icefish

“…Even after the evolution of these phenotypes, icefish still exhibit limited cardiac performance, with less than 10% of the oxygen carrying capacity of red-blooded notothenioids (Holeton 1970) and far larger cardiac energy expenditures (Tota et al 1991;Tota and Gattuso 1996). Given these biological limitations, the loss of Hb in icefish was often considered to be maladaptive (Sidell and O'Brien 2006), although recent work has proposed alternative hypotheses related to adaptive changes in the presence of sparse iron and alternative functional roles for partial Hb fragments (Corliss et al 2019). Regardless of the evolutionary mechanism behind the loss, the derived physiology stemming from the lack of Hb is predicted to limit icefishes' adaptive potential to migrate to warmer waters or to respond to rapidly changing ocean temperatures.…”

Quantitative Proteomics and Network Analysis of Differentially Expressed Proteins in Proteomes of Icefish Muscle Mitochondria Compared with Closely Related Red-Blooded Species

“…To understand the role of haemoglobin, it can be useful to examine eukaryotic systems that express this important protein at different levels. There is a wide range of evidence that suggests Hb has dynamic locations in cell, neurons, endothelial cells, mitochondria, and vascular expression [ 9 , 10 , 11 , 12 , 13 ]. Previously, we have shown that haemoglobin proteins are located in the mitochondrion and both direct and indirect links have been established between mitochondria function and Hb expression [ 10 , 14 , 15 ].…”