The Antarctic hemoglobinless icefish, fifty five years later: A unique cardiocirculatory interplay of disaptation and phenotypic plasticity

The teleostean Channichthyidae (icefish), endemic stenotherms of the Antarctic waters, perennially at ornear freezing, represent a unique example of disaptation among adult vertebrates for their loss of functionaltraits, particularly hemoglobin (Hb) and, in some species, cardiac myoglobin (Mb), once considered to beessential-life oxygen-binding chromoproteins. Conceivably, this stably frigid, oxygen-rich habitat haspermitted high tolerance of disaptation, followed by subsequent adaptive recovery based on gene expressionreprogramming and compensatory responses, including an alternative cardio-circulatory design, Hb-freeblood and Mb-free cardiac muscle. This review revisits the functional significance of the multilevel cardiocirculatorycompensations (hypervolemia, near-zero hematocrit and low blood viscosity, large borecapillaries, increased vascularity with great capacitance, cardiomegaly with very large cardiac output, highblood flow with low systemic pressure and systemic resistance) that counteract the challenge of hypoxemichypoxia by increasing peripheral oxygen transcellular movement for aerobic tissues, including themyocardium. Reconsidered in the context of recent knowledge on both polar cold adaptation and the newquestions related to the advent of nitric oxide (NO) biology, these compensations can be interpreted eitheraccording to the “loss-without-penalty” alternative, or in the context of an excessive environmental oxygensupply at low cellular cost and oxygen requirement in the cold. Therefore, rather than reflecting oxygenlimitation, several traits may indicate structural overcompensation of oxygen supply reductions at cell/tissuelevels. At the multilevel cardio-circulatory adjustments, NO is revealing itself as a major integrator,compensating disaptation with functional phenotypic plasticity, as illustrated by the heart paradigm. BesideNOS-dependent NO generation, recent knowledge concerning Hb/Mb interplay with NO and nitrite hasrevealed unexpected functions in addition to the classical respiratory role of these proteins. In fact, nitrite, amajor biologic reservoir of NO, generates it through deohyHb- and deoxyMb-dependent nitrite reduction,thereby regulating hypoxic vasodilation, cellular respiration and signalling. We suggest that both Hb and Mbare involved as nitrite reductases under hypoxic conditions in a number of cardiocirculatory processes. Onthe whole, this opens new horizons in environmental and evolutionary physiology