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An atlas of plasma-accessible carbonic anhydrase availability in the model teleost, the rainbow trout

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Abstract

The unique teleost oxygenation system that permits enhanced oxygen unloading during stress comprises three main characteristics: pH-sensitive haemoglobin, red blood cell (RBC) intracellular pH (pHi) protection, and a heterogeneous distribution of plasma-accessible carbonic anhydrase (paCA). A heterogeneous distribution of paCA is essential; its presence permits enhanced oxygen unloading during stress, while its absence at the gills maintains conditions for oxygen uptake by pH-sensitive haemoglobins. We hypothesised that paCA would be absent in all four gill arches, as has been previously indicated for arch two, and that paCA would be present in all other tissues. Through a suite of biochemical and molecular methods, we confirmed the absence of paCA from all four arches. We also found evidence for paCA in nine other tissues and a lack of paCA availability in the stomach. Expression was highly variable between tissues and suggests these differences may be associated with their respective metabolic activities. Additionally, we analysed the specific CA-IV isoform expressed within each tissue and showed almost complete separation of expression between tissues; CA-IVa was detected in the heart, brain, anterior intestine, and liver, whereas CA-IVb was detected in all intestine sections, pyloric caeca, kidney, and white muscle. This adds to a growing collection of work suggesting CA-IVa and b play divergent roles in gas exchange and ion/acid–base balance, respectively. The current study represents the first comprehensive atlas of paCA availability within the circulatory system of the model teleost, rainbow trout, and fills important gaps in our knowledge of this unique oxygenation system.

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Data availability

Data are available in supplementary materials.

Abbreviations

β-NHE:

Beta-adrenergically stimulated sodium proton exchanger

CA:

Carbonic anhydrase

CA-IV:

Carbonic anhydrase IV

cDNA:

Complementary deoxyribonucleic acid

CO2 :

Carbon dioxide

GPI:

Glycophosphatidylinositol anchor

Hb:

Haemoglobin

HCO3 − :

Bicarbonate

mRNA:

Messenger ribonucleic acid

O2 :

Oxygen

paCA:

Plasma-accessible carbonic anhydrase

PCO2 :

Partial pressure of carbon dioxide

pHe:

Extracellular pH

pHi:

Intracellular pH

PI-PLC:

Phosphatidylinositol specific phospholipase C

PICA:

Plasma inhibitors of carbonic anhydrase

qPCR:

Quantitative polymerase chain reaction

RBC:

Red blood cell

SDS:

Sodium dodecyl sulphate

t1/2 :

Half-time

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Funding

This study was supported by a Natural Sciences and Engineering Research Council (NSERC) Discovery grant (RGPIN-2018-04172).

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Authors and Affiliations

  1. University of British Columbia, Vancouver, BC, V6T 1Z4, Canada

    Charlotte Nelson, Angelina M. Dichiera, Ellen H. Jung & Colin J. Brauner

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  1. Charlotte Nelson
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  2. Angelina M. Dichiera
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  3. Ellen H. Jung
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  4. Colin J. Brauner
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Contributions

The authors confirm contribution to the paper as follows: study conception and design: C. Nelson and C. J. Brauner; data collection: C. Nelson, E. H. Jung, and A. M. Dichiera; analysis and interpretation of results: C. Nelson, A. M. Dichiera, and C. J. Brauner; draft manuscript preparation: C. Nelson. All authors reviewed the results and approved the final version of the manuscript. We would like to acknowledge and thank Benjamin Mills for creating the illustrations used in Fig. 4 of this manuscript.

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Correspondence to Charlotte Nelson.

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Summary Statement

In this study we developed an atlas of plasma accessible carbonic anhydrase availability in rainbow trout, filling gaps in our knowledge of how the unique teleost respiratory system functions.

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Nelson, C., Dichiera, A.M., Jung, E.H. et al. An atlas of plasma-accessible carbonic anhydrase availability in the model teleost, the rainbow trout. J Comp Physiol B 193, 293–305 (2023). https://doi.org/10.1007/s00360-023-01484-7

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