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Magnesium transport in the aglomerular kidney of the Gulf toadfish (Opsanus beta)

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Abstract

Despite having an aglomerular kidney, Gulf toadfish can survive in water ranging from nearly fresh up to 70 parts per thousand salinity. In hyperosmotic environments, the major renal function is to balance the passive Mg2+ load from the environment with an equal excretion. However, the molecular transporters involved in Mg2+ secretion are poorly understood. We investigated whether environmental MgCl2 alone or in combination with elevated salinity affected transcriptional regulation of genes classically involved in renal Mg2+ secretion (slc41a1, slc41a3, cnnm3) together with three novel genes (trpm6, trpm7, claudin-19) and two isoforms of the Na+/K+-ATPase α-subunit (nka-α1a, nka-α1b). First, toadfish were acclimated to 5, 9, 35, or 60 ppt water (corresponding to ~ 7, 13, 50 and 108 mmol L−1 ambient [Mg2+], respectively) and sampled at 24 h or 9 days. Next, the impact of elevated ambient [Mg2+] was explored by exposing toadfish to control (50 mmol L−1 Mg2+), or elevated [Mg2+] (100 mmol L−1) at a constant salinity for 7 days. Mg2+ levels in this experiment corresponded with levels in control and hypersaline conditions in the first experiment. A salinity increase from 5 to 60 ppt stimulated the level of all investigated transcripts in the kidney. In Mg2+-exposed fish, we observed a 14-fold increase in the volume of intestinal fluids and elevated plasma osmolality and [Mg2+], suggesting osmoregulatory challenges. However, none of the renal gene targets changed expression compared with the control group. We conclude that transcriptional regulation of renal Mg2+ transporters is induced by elevated [Mg2+] in combination with salinity rather than elevated ambient [Mg2+] alone.

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Acknowledgements

The author(s) acknowledge the Danish Molecular Biomedical Imaging Center (DaMBIC, University of Southern Denmark) for the use of the bioimaging facilities. We wish to thank Tony Jr. and Captain Jorge for providing toadfish for the present study.

Funding

S.S.M. received support from the Danish Research Council for Independent Research (DFF‐4181‐00020). M.G. is a Maytag Professor of Ichthyology.

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Contributions

Conceptualization: S.S.M, M.G.; Methodology: M.G., S.S.M.; Formal analysis: N.G.W.H., M.B., S.S.M.; Investigation: N.G.W.H., M.B.E., R.M.H, L.S.S, M.G.; Resources: M.G.; Writing—original draft: N.G.W.H., S.S.M.; Writing—review and editing: M.B., M.G., R.M.H., L.S.S., M.B.E.; Visualization: M.B., S.S.M.; Supervision: S.S.M., M.G.; Project administration: S.S.M., M.G.; Funding acquisition: S.S.M., M.G.

Corresponding author

Correspondence to Steffen S. Madsen.

Additional information

Communicated by B. Pelster.

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Hansen, N.G.W., Madsen, S.S., Brauckhoff, M. et al. Magnesium transport in the aglomerular kidney of the Gulf toadfish (Opsanus beta). J Comp Physiol B 191, 865–880 (2021). https://doi.org/10.1007/s00360-021-01392-8

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  • DOI: https://doi.org/10.1007/s00360-021-01392-8

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