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

Author:

Damsgaard Christian1ORCID,Lauridsen Henrik2ORCID,Harter Till S3ORCID,Kwan Garfield T3ORCID,Thomsen Jesper S4ORCID,Funder Anette MD5,Supuran Claudiu T6,Tresguerres Martin3ORCID,Matthews Philip GD1ORCID,Brauner Colin J1

Affiliation:

1. Department of Zoology, University of British Columbia, Vancouver, Canada

2. Department of Clinical Medicine, Aarhus University, Aarhus, Denmark

3. Scripps Institution of Oceanography, UC San Diego, La Jolla, United States

4. Department of Biomedicine, Aarhus University, Aarhus, Denmark

5. Department of Forensic Medicine, Aarhus University, Aarhus, Denmark

6. Università degli Studi di Firenze, Neurofarba Department, Sezione di Scienze Farmaceutiche, Florence, Italy

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.

Funder

Carlsbergfondet

National Science Foundation

Velux Fonden

Natural Sciences and Engineering Research Council of Canada

Publisher

eLife Sciences Publications, Ltd

Subject

General Immunology and Microbiology,General Biochemistry, Genetics and Molecular Biology,General Medicine,General Neuroscience

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