PO2 profiles in the retina of the hemoglobin-less icefishes

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The retina of vertebrates has one of the highest O2 demands and requires a constant O2 supply. Four general types of retinal circulations have been described for O2 delivery in extant vertebrates: 1) sole reliance on the choriocapillaris; 2) capillaries penetrating the retina; 3) capillarization of the inner side of the retina; and 4) O2 secretion. Oxygen secretion is based on acid secretion into the blood resulting in a potent unloading of O2 from so-called Root effect hemoglobins (Hb), which is augmented by venous to arterial O2 diffusion in a vascular rete lining the back side of the retina. This choroid rete mirabile (CRM) allows O2 delivery at super-atmospheric pressure in the avascular retina of some fishes that have the thickest retinae and some of the largest eyes (relative to body size) of all extant vertebrates. The suborder Notothenioidei, which consists of Antarctic and sub-Antarctic fishes, provides a model system to unravel how the interactions between Hb function and retinal vascularity evolved to produce modern fish eyes. While several phyletically basal notothenioids have been shown to display similar ocular arrangements as in other Perciform species containing a CRM, more phyletically derived notothenioids have highly reduced CRM or have lost it completely. Of particular interest are the species of the family Channichthyidae, icefishes, that are unique among adult vertebrates in possessing pale white blood containing only few vestigial immature erythrocytes and no Hb. Without Hb, O2 secretion is not functional, and icefishes have been demonstrated to possess heavily increased pre-retinal capillarization most probably to maintain retinal oxygenation and preserve large eyes and thick retinae. However, whether available O2 at different retinal levels actually follows the degree of vascularization has not been tested.

Using thin O2 sensors, we measured profiles of partial pressure of O2 (PO2) in the retina of six species of icefishes, two species of related, but red-blooded dragonfishes (Bathydraconidae), and four species of more distantly related notothens (Nototheniidae). Arterial PO2 was statistically significantly higher in icefishes than in notothens [t-test; p = 0.0066 (n = 3); PaO2 = 16.64 ± 3.84 kPa in Chaenocephalus aceratus; PaO2 = 4.42 ± 1.40 kPa in Notothenia coriiceps]. In general, pre-retinal PO2 was high in icefishes (19.20 ± 6.35 kPa in C. aceratus), approaching the theoretical O2 solubility limit without O2 secretion. The PO2 level decreased towards the outer portion of the retina, but with a small peak on the choroid side of the retina, possibly due to a vestigial choriocapillaris. In notothens displaying Root effect, pre-retinal PO2 was slightly lower (12.07 ± 5.12 kPa in N. coriiceps) but increased to a super-atmospheric level on the outer portion of the retina (52.25 ± 32.46 kPa in N. coriiceps).

Our results demonstrate that retinal PO2 is dictated by vascularization in the Hb-deprived icefishes, leading to a unique reversal in the retinal oxygen profile.
TidsskriftF A S E B Journal
StatusUdgivet - 2019

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