Abstract
A large amount of data is currently available on the adaptive mechanisms of polar bony fish hemoglobins, but structural information on those of cartilaginous species is scarce. This study presents the first characterisation of the hemoglobin system of one of the longest-living vertebrate species (392 ± 120 years), the Arctic shark Somniosus microcephalus. Three major hemoglobins are found in its red blood cells and are made of two copies of the same α globin combined with two copies of three very similar β subunits. The three hemoglobins show very similar oxygenation and carbonylation properties, which are unaffected by urea, a very important compound in marine elasmobranch physiology. They display identical electronic absorption and resonance Raman spectra, indicating that their heme-pocket structures are identical or highly similar. The quaternary transition equilibrium between the relaxed (R) and the tense (T) states is more dependent on physiological allosteric effectors than in human hemoglobin, as also demonstrated in polar teleost hemoglobins. Similar to other cartilaginous fishes, we found no evidence for functional differentiation among the three isoforms. The very similar ligand-binding properties suggest that regulatory control of O2 transport may be at the cellular level and that it may involve changes in the cellular concentrations of allosteric effectors and/or variations of other systemic factors. The hemoglobins of this polar shark have evolved adaptive decreases in O2 affinity in comparison to temperate sharks.
Highlights
Organisms living in polar environments are exposed to strong environmental constraints
During the TUNU-V expedition in August 2013, specimens of the Greenland shark S. microcephalus were caught by long lines, set at 700 m or more, in Tyrolerfjord, NE Greenland (74N, 21W)
All procedures were conducted in accordance with the Animal Welfare Act and were approved by the Arctic University of Norway, Norway
Summary
Organisms living in polar environments are exposed to strong environmental constraints. Temperature is often the main environmental stress or adaptation driver over timescales ranging from hours to millennia. Arctic regions are inhabited by cold-adapted species, which may be either stenothermal or eurythermal, likely depending on ambient temperature variability and evolutionary history [1, 2]. Eurythermal species predominate, because the continuous coastlines from tropical to polar latitudes increase the opportunities for north-south migrations. The constant water temperature in the Southern Ocean, where fluctuations rarely exceed 2 ̊C, favoured the evolution of stenothermal animal life [3, 4]. In the Arctic, cartilaginous fishes, such as sharks and skates, are notably present, with about 8% of the species [5]
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