Functional support for a novel mechanism that enhances tissue oxygen extraction in a teleost fish

Author:

Harter T. S.1ORCID,Zanuzzo F. S.2,Supuran C. T.3,Gamperl A. K.2,Brauner C. J.1

Affiliation:

1. Department of Zoology, The University of British Columbia, Vancouver, British Columbia, Canada V6T 1Z4

2. Department of Ocean Sciences, Memorial University of Newfoundland, St John's, Newfoundland, Canada A1C 5S7

3. NEUROFARBA Department, Università degli Studi di Firenze, Florence, Italy

Abstract

A successful spawning migration in salmon depends on their athletic ability, and thus on efficient cardiovascular oxygen (O 2 ) transport. Most teleost fishes have highly pH-sensitive haemoglobins (Hb) that can release large amounts of O 2 when the blood is acidified at the tissues. We hypothesized that plasma-accessible carbonic anhydrase (paCA; the enzyme that catalyses proton production from CO 2 ) is required to acidify the blood at the tissues and promote tissue O 2 extraction. Previous studies have reported an elevated tissue O 2 extraction in hypoxia-acclimated teleosts that may also be facilitated by paCA. Thus, to create experimental contrasts in tissue O 2 extraction, Atlantic salmon were acclimated to normoxia or hypoxia (40% air saturation for more than six weeks), and the role of paCA in enhancing tissue O 2 extraction was tested by inhibiting paCA at rest and during submaximal exercise. Our results show that: (i) in both acclimation groups, the inhibition of paCA increased cardiac output by one-third, indicating a role of paCA in promoting tissue O 2 extraction during exercise, recovery and at rest; (ii) the recruitment of paCA was plastic and increased following hypoxic acclimation; and (iii) maximal exercise performance in salmon, and thus a successful spawning migration, may not be possible without paCA.

Funder

Company of Biologists

Natural Sciences and Engineering Research Council of Canada

Canadian Society of Zoologists

Ocean Frontier Institute

Publisher

The Royal Society

Subject

General Agricultural and Biological Sciences,General Environmental Science,General Immunology and Microbiology,General Biochemistry, Genetics and Molecular Biology,General Medicine

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