Hemoglobin Polymerization in Red Blood Cells of Marine Fishes: A Case of Adaptive Phenotypic Plasticity?

We investigated the occurrence of the unusual phenomenon of hemoglobin polymerization in a 10-year survey of 47 species of fishes. Similar to human sickle cell disease, hemoglobin polymers in fish red blood cells can cause distortion or sickling under low oxygen and low pH. We sampled fish from three geographic areas, including the east and west coasts of the Atlantic Ocean and the Gulf of Mexico. Fifteen species spanning five orders and nine families exhibited hemoglobin polymerization in vitro, with a majority in or related to Gadiformes, as well as species within Notocanthiformes, Perciformes, and Scorpianiformes. Atlantic cod, Gadus morhua, also showed the trait in vivo. Light and transmission electron microscopy confirmed the presence of hemoglobin polymers at the cellular level, but the morphology of hemoglobin polymers and rates of polymerization varied across species. Hemoglobin polymerization in red blood cells in vitro was pH dependent and reversible. For two species, G. morhua and Opsanus tau, >60% and >40% of all red blood cells contained hemoglobin polymers at pH 7.6, while 100% and 90% of red blood cells polymerized at pH 6.96, respectively. In both species, recovery of 60%-70% of red blood cells occurred within 45 minutes when pH increased from 6.96 to 7.99. From these results we conclude that hemoglobin polymerization is present in a broad range of fish taxa occupying wide biogeographical ranges and habitats and that it is oxygen and pH sensitive. The physiology and adaptive significance of hemoglobin polymerization in fishes remain unclear, but as oceans and coastal environments become more hypoxic and hypercapnic, this trait may have the potential to affect fish survival.