Molecular basis of mitochondrial form and function in the hearts of antarctic notothenioids that vary in the expression of hemoglobin and myoglobin

Abstract

Antarctic icefish (suborder Notothenioidei, family Channichthyidae) do not express hemoglobin (Hb), and 6 of the 16 members of this family do not express myoglobin (Mb) in their cardiac muscle. The loss of Hb and Mb correlates with an increase in mitochondrial volume density, a decrease in the mitochondrial surface-to-volume ratio and a decrease in the surface density of inner mitochondria) membranes in the hearts of icefishes compared to red-blooded notothenioids. We sought to understand the molecular mechanisms that regulate differences in mitochondrial density and morphology among the hearts of the notothenioids Notothenia coriiceps (+Hb/+Mb), Gobionotothen gibberifrons (+Hb/+Mb), Chaenocephalus aceratus ( -Hb/-Mb) and Chionodraco rastrospinosus ( -Hb/+Mb). We also sought to determine if alterations in mitochonmdrial structure affect mitochondrial function. Our results indicate that high mitochondrial densities in icefish hearts may be maintained by a novel pathway of mitochondrial biogenesis leading to an increase in the size, rather than number of mitochondria. The expression of mitofilin, which regulates mitochondrial cristae morphology, correlates with differences in the architecture of inner mitochondrial membranes between C. aceratus and N. coriiceps. Moreover, differences in mitochondrial morphology among hearts of G. gibberifrons, C. rastrospinosus and C. aceratus are associated with differences in oxygen consumption rates of isolated mitochondria.