A novel acidification mechanism for greatly enhanced oxygen supply to the fish retina.

Christian Damsgaard,Anette Md Funder,Henrik Lauridsen,Philip Gd Matthews,Martin Tresguerres,Jesper S Thomsen,Till S Harter,Claudiu T Supuran,Garfield T Kwan,Colin J Brauner

doi:10.7554/elife.58995

Abstract

Previously, we showed that the evolution of high acuity vision in fishes was directly associated with their unique pH-sensitive hemoglobins that allow O2 to be delivered to the retina at PO2s more than ten-fold that of arterial blood (Damsgaard et al., 2019). Here, we show strong evidence that vacuolar-type H+-ATPase and plasma-accessible carbonic anhydrase in the vascular structure supplying the retina act together to acidify the red blood cell leading to O2 secretion. In vivo data indicate that this pathway primarily affects the oxygenation of the inner retina involved in signal processing and transduction, and that the evolution of this pathway was tightly associated with the morphological expansion of the inner retina. We conclude that this mechanism for retinal oxygenation played a vital role in the adaptive evolution of vision in teleost fishes.

Highlights

The retina of vertebrates, containing the light-sensitive photoreceptors required for visual perception, has a very high metabolic rate that must be supported by an adequate supply of O2 (Linsenmeier and Braun, 1992)
To support such a high O2 demand, most tissues possess a dense network of capillaries that minimize diffusion distances, facilitating the transfer of O2 from the red blood cells (RBCs) to the respiring mitochondria
H+s do not rapidly cross the red blood cell membrane and must be combined with HCO3À to form CO2 (HCO3À dehydration) that readily diffuses across the RBC membrane (Brauner et al, 2019). This dehydration reaction is slow relative to rates of blood capillary transit, so we propose that a catalytic plasma-accessible carbonic anhydrase is required to take advantage of vacuolar-type H+-ATPase (VHA) H+-excretion for RBC acidification

Summary

Introduction

The retina of vertebrates, containing the light-sensitive photoreceptors required for visual perception, has a very high metabolic rate that must be supported by an adequate supply of O2 (Linsenmeier and Braun, 1992). To support such a high O2 demand, most tissues possess a dense network of capillaries that minimize diffusion distances, facilitating the transfer of O2 from the red blood cells (RBCs) to the respiring mitochondria.

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