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Na+/HCO3− cotransporter 1 (nbce1) isoform gene expression during smoltification and seawater acclimation of Atlantic salmon

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Abstract

The life history of Atlantic salmon (Salmo salar) includes an initial freshwater phase (parr) that precedes a springtime migration to marine environments as smolts. The development of osmoregulatory systems that will ultimately support the survival of juveniles upon entry into marine habitats is a key aspect of smoltification. While the acquisition of seawater tolerance in all euryhaline species demands the concerted activity of specific ion pumps, transporters, and channels, the contributions of Na+/HCO3− cotransporter 1 (Nbce1) to salinity acclimation remain unresolved. Here, we investigated the branchial and intestinal expression of three Na+/HCO3− cotransporter 1 isoforms, denoted nbce1.1, -1.2a, and -1.2b. Given the proposed role of Nbce1 in supporting the absorption of environmental Na+ by ionocytes, we first hypothesized that expression of a branchial nbce1 transcript (nbce1.2a) would be attenuated in salmon undergoing smoltification and following seawater exposure. In two separate years, we observed spring increases in branchial Na+/K+-ATPase activity, Na+/K+/2Cl− cotransporter 1, and cystic fibrosis transmembrane regulator 1 expression characteristic of smoltification, whereas there were no attendant changes in nbce1.2a expression. Nonetheless, branchial nbce1.2a levels were reduced in parr and smolts within 2 days of seawater exposure. In the intestine, gene transcript abundance for nbce1.1 increased from spring to summer in the anterior intestine, but not in the posterior intestine or pyloric caeca, and nbce1.1 and -1.2b expression in the intestine showed season-dependent transcriptional regulation by seawater exposure. Collectively, our data indicate that tissue-specific modulation of all three nbce1 isoforms underlies adaptive responses to seawater.

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Acknowledgements

We appreciate the excellent laboratory assistance and fish care provided by Amy Regish and Dan Hall during the course of this study.

Funding

This work was supported by the National Science Foundation (IOS-1755131 to JPB). Any use of trade, product, or firm names is for descriptive purposes only and does not imply endorsement by the US Government.

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Authors and Affiliations

  1. Department of Biology, Skidmore College, 815 N. Broadway, Saratoga Springs, NY, 12866, USA

    Jason P. Breves, Ian S. McKay, Victor Koltenyuk & Nastasia N. Nelson

  2. Biological Sciences Department, Center for Coastal Marine Sciences, California Polytechnic State University, San Luis Obispo, CA, 93407, USA

    Sean C. Lema

  3. U.S. Geological Survey, Eastern Ecological Science Center, Conte Anadromous Fish Research Laboratory, One Migratory Way, Turners Falls, MA, 01376, USA

    Stephen D. McCormick

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  1. Jason P. Breves
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  2. Ian S. McKay
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Correspondence to Jason P. Breves.

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Breves, J.P., McKay, I.S., Koltenyuk, V. et al. Na+/HCO3− cotransporter 1 (nbce1) isoform gene expression during smoltification and seawater acclimation of Atlantic salmon. J Comp Physiol B 192, 577–592 (2022). https://doi.org/10.1007/s00360-022-01443-8

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