The Greenland shark Somniosus microcephalus—Hemoglobins and ligand-binding properties

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.

Advancing Research for the Management of Long-Lived Species: A Case Study on the Greenland Shark

“…Scar patterns and external markings may be used to identify individuals over short time periods (Devine et al, 2018), but these may also change or disappear with age (Robbins and Fox, 2012). External markers (e.g., Floy tags) facilitate identification (Section "Demographics and Life History"), however, studies should determine the average duration of tag retention by target species.…”

“…A recent study on the whole blood of Greenland sharks noted that their blood properties (high oxygen affinity and low Bohr effect) were typical of sluggish elasmobranchs (Herbert et al, 2017). However, using isolated haemoglobins, the blood was found to have a relatively low affinity and consist of three hemoglobin isoforms with no functional differences (Russo et al, 2017). This analysis suggested that cellular changes in allosteric effectors may be important for controlling the O 2 transport properties of the blood.…”

“…Systematic surveys of local traditional knowledge and accounts from fishermen could help fill gaps in distribution, while the expansion of BRUV surveys could explore differences in relative abundances among sites, and seasonal BRUV surveys could help determine cyclic patterns in distribution. Although scar patterns and the coloration of individuals may change over time (Robbins and Fox, 2012), the use of colored Floy tags or other external markers could provide reliable long-term identification for both BRUVs and fisherymediated surveys ( Table 2). By modifying conventional mark-recapture models to integrate auxiliary data derived from acoustic or satellite telemetry, the effects of low recapture rates can be offset, resulting in more precise estimates of demographic parameters such as apparent survival and abundance (Dudgeon et al, 2015).…”