The interplay among cardiac ultrastructure, metabolism and the expression of oxygen-binding proteins in Antarctic fishes

We examined heart ventricle from three species of Antarctic fishes that var y in their expression of oxygen-binding proteins to investigate how some of these fishes maintain cardiac function despite the loss of hemoglobin (Hb) and/or myoglobin (Mb), We quantified ultrastructural features and enzymati c indices of metabolic capacity in cardiac muscle from Gobionotothen gibber ifrons, which expresses both Hb and Mb, Chionodraco rastrospinosus, which l acks Hb but expresses Mb, and Chaenocephalus aceratus, which lacks both I-I b and Mb, The most striking difference in cellular architecture of the hear t among these species is the percentage of cell volume occupied by mitochon dria, V-v(mit,f), which is greatest in Chaenocephalus aceratus (36.53+/-2.0 7), intermediate in Chionodraco rastrospinosus (20.10+/-0.74) and lowest in G, gibberifrons (15.87+/-0.74). There are also differences in mitochondria l morphologies among the three species, The surface area of inner mitochond rial membrane per volume of mitochondria, S-v(imm,mit), varies inversely wi th mitochondrial volume density so that Sv(imm,mit) is greatest in G, gibbe rifrons (29.63+/-1.62 mu m(-1)), lower in Chionodraco rastrospinosus (21.52 +/-0.69 mu m(-1)) and smallest in Chaenocephalus aceratus (20.04+/-0.79 mu m(-1)). The surface area of mitochondrial cristae per gram of tissue, howev er, is greater in Chaenocephalus aceratus than in G, gibberifrons and Chion odraco rastrospinosus, whose surface areas are similar, Despite significant ultrastructural differences, oxidative capacities, estimated from measurem ents of maximal activities per gram of tissue of enzymes from aerobic metab olic pathways, are similar among the three species. The combination of ultr astructural and enzymatic data indicates that there are differences in the density of electron transport chain proteins within the inner mitochondrial membrane; proteins are less densely packed within the cristae of hearts fr om Chaenocephalus aceratus than in the other two species, High mitochondria l densities within hearts from species that lack oxygen-binding proteins ma y help maintain oxygen flux by decreasing the diffusion distance between th e ventricular lumen and mitochondrial membrane, Also, high mitochondrial de nsities result in a high intracellular lipid content, which may enhance oxy gen diffusion because of the higher solubility of oxygen in lipid compared with cytoplasm, These results indicate that features of cardiac myocyte arc hitecture in species lacking oxygen-binding proteins may maintain oxygen fl ux, ensuring that aerobic metabolic capacity is not diminished and that car diac function is maintained.