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First published online July 6, 2005
Journal of Experimental Biology 208, 2719-2729 (2005)
Published by The Company of Biologists 2005
doi: 10.1242/jeb.01688

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Gene expression after freshwater transfer in gills and opercular epithelia of killifish: insight into divergent mechanisms of ion transport

Graham R. Scott^1,*, James B. Claiborne², Susan L. Edwards^2,3, Patricia M. Schulte¹ and Chris M. Wood⁴

¹ Department of Zoology, University of British Columbia, Vancouver BC, Canada V6T 1Z4
² Department of Biology, Georgia Southern University, Statesboro, GA 30460-8042, USA
³ Department of Physiology and Pharmacology, James Cook University, Cairns, QLD 4879, Australia
⁴ Department of Biology, McMaster University, Hamilton ON, Canada L8S 4K1

^* Author for correspondence (e-mail: scott{at}zoology.ubc.ca)

Accepted 17 May 2005

We have explored the molecular basis for differences in physiological function between the gills and opercular epithelium of the euryhaline killifish Fundulus heteroclitus. These tissues are functionally similar in seawater, but in freshwater the gills actively absorb Na⁺ but not Cl^–, whereas the opercular epithelium actively absorbs Cl^– but not Na⁺. These differences in freshwater physiology are likely due to differences in absolute levels of gene expression (measured using real-time PCR), as several proteins important for Na⁺ transport, namely Na⁺,H⁺-exchanger 2 (NHE2), carbonic anhydrase 2 (CA2), Na⁺,HCO₃^–cotransporter 1, and V-type H⁺-ATPase, were expressed at 3- to over 30-fold higher absolute levels in the gills. In gills, transfer from 10% seawater to freshwater increased the activity of Na⁺,K⁺-ATPase by twofold (from 12 h to 7 days), increased the expression of NHE2 (at 12 h) and CA2 (from 12 h to 7 days), and decreased the expression of NHE3 (from 12 h to 3 days). In opercular epithelium, NHE2 was not expressed; furthermore, Na⁺,K⁺-ATPase activity was unchanged after transfer to freshwater, CA2 mRNA levels decreased, and NHE3 levels increased. Consistent with their functional similarities in seawater, killifish gills and opercular epithelium expressed Na⁺,K⁺-ATPase _1a, Na⁺,K⁺,2Cl^–cotransporter 1 (NKCC1), cystic fibrosis transmembrane conductance regulator (CFTR) Cl^– channel and the signalling protein 14-3-3a at similar absolute levels. Furthermore, NKCC1 and CFTR were suppressed equally in each tissue after freshwater transfer, and 14-3-3a mRNA increased in both. These results provide insight into the mechanisms of ion transport by killifish gills and opercular epithelia, and demonstrate a potential molecular basis for the differences in physiological function between these two organs.

Key words: Fundulus heteroclitus, carbonic anhydrase, Na⁺, H⁺-exchanger, Na⁺, HCO₃^–cotransporter, fish

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