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The effects of gill remodeling on transepithelial sodium fluxes and the distribution of presumptive sodium-transporting ionocytes in goldfish (Carassius auratus)

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Abstract

Goldfish, Carassius auratus, adaptively remodel their gills in response to changes in ambient oxygen and temperature, altering the functional lamellar surface area to balance the opposing requirements for respiration and osmoregulation. In this study, the effects of thermal- and hypoxia-mediated gill remodeling on branchial Na+ fluxes and the distribution of putative Na+-transporting ionocytes in goldfish were assessed. When assessed either in vitro (isolated gill arches) or in vivo at a common water temperature, the presence of an interlamellar cell mass (ILCM) in fish acclimated to 7°C clearly decreased Na+ efflux across the gill relative to fish maintained at 25°C and lacking an ILCM. However, loss of the ILCM in 7°C-acclimated fish exposed to hypoxia led to a decrease in Na+ efflux (assessed under hypoxic conditions) despite the apparent large increases in functional lamellar surface area. Goldfish possessing an ILCM were able to sustain Na+ uptake, albeit at a lower rate matched to efflux, owing to the re-distribution of ionocytes expressing genes thought to be involved in Na+ uptake [Na+/H+ exchanger isoform 3 (NHE3) and V- type H+-ATPase] to the edge of the ILCM where they can establish contact with the surrounding environment. NHE-expressing cells co-localized with Na+/K+-ATPase expression, suggesting a role for NHE in Na+-uptake in the goldfish. Implications of the ILCM on ion fluxes in the goldfish are discussed.

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Acknowledgments

This research was supported by NSERC of Canada Discovery and Research Tools and Infrastructure grants to SFP. We thank Andrew Ochalski for technical guidance for the microscopy experiments and Bill Fletcher for his dedication to animal care.

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  1. Department of Biology, University of Ottawa, 30 Marie Curie, Ottawa, ON, K1N 6N5, Canada

    Julia C. Bradshaw, Yusuke Kumai & Steve F. Perry

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  1. Julia C. Bradshaw
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  2. Yusuke Kumai
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  3. Steve F. Perry
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Correspondence to Steve F. Perry.

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Communicated by H.V. Carey.

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Bradshaw, J.C., Kumai, Y. & Perry, S.F. The effects of gill remodeling on transepithelial sodium fluxes and the distribution of presumptive sodium-transporting ionocytes in goldfish (Carassius auratus). J Comp Physiol B 182, 351–366 (2012). https://doi.org/10.1007/s00360-011-0618-7

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  • DOI: https://doi.org/10.1007/s00360-011-0618-7

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