Cationic control of O₂ affinity in lugworm erythrocruorin

Abstract

The erythrocruorins (extracellular haemoglobins from annelids¹) have molecular weights of 3–4 ×l0⁶, contain 60–192 O₂-binding haem moieties per molecule and are much more complex than the tetrameric vertebrate haemoglobins^1–5. However, they perform the same function, carrying O₂ from the respiratory surfaces to the tissues, and exhibit similar coopera-tivity in O₂ binding and inhibitory heterotropic interactions between O₂- and proton-binding sites (Bohr effects), although these functions show greater adaptive variation than in the vertebrate pigments^2,3. Whereas erythrocruorin–O₂ affinity is insensitive to the anionic organic phosphate cofactors like glycerate-2,3-bisphosphate and ATP^1–3, which depress the O₂ affinity of vertebrate haemoglobin inside the red blood cells, it is increased by inorganic salts^6–8. This effect is important physiologically because annelids lack significant capacity for osmotic regulation and experience large fluctuations in blood electrolyte levels^8,9.I show here that, in contrast to the situation in man, where anionic cofactors and protons decrease haemoglobin–O₂ affinity by specifically depressing the O₂ association equilibrium constant of the pigment in the deoxygenated state^10–13, inorganic cations govern the O₂ affinity of erythrocruorin from the burrowing, intertidal lugworm, Arenicola marina, by preferentially modifying the association constant of the (almost fully) oxygenated form. In contrast to the vertebrate mechanism, riftich optimizes O₂ unloading in the tissues, this alternative control mechanism in erythrocruorin seems to be adaptive to O₂ loading at the low O₂ tensions generally characteristic of the microenvironments of erythrocruorin-bearing annelids^1–3.