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Distribution of Na+/K+-ATPase-immunoreactive ionocytes varies between two superorders of ray-finned fish: Ostariophysi and Acanthopterygii

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Abstract

Ray-finned fishes of the superorder Ostariophysi are primarily freshwater (FW), and normally stenohaline. Differently, fishes of the superorder Acanthopterygii are essentially marine, and frequently euryhaline, with some secondary FW. Na+/K+-ATPase-immunoreactive ionocytes were localized in the branchial epithelia of 4 species of Ostariophysi and 3 of Acanthopterygii. The Ostariophysi grass carp (Ctenopharyngodon idella, Cypriniformes), twospot Astyanax (Astyanax bimaculatus) and piracanjuba (Brycon orbignyanus), Characiformes, and the jundiá (Rhamdia quelen, Siluriformes), all from FW, displayed ionocytes in the filament plus secondary lamellae (F + SL). In their turn, all the three species of Acanthopterygii showed immunoreactive ionocytes in the filaments only (F). They were the Nile tilapia (Oreochromis niloticus, Cichliformes) in FW, the dog snapper (Lutjanus jocu, Perciformes) in seawater (SW), and the green puffer (Sphoeroides greeleyi, Tetraodontiformes) in SW. Ionocytes normally extend their distribution to the secondary lamellae (F + SL) in Ostariophysi. In Acanthopterygii, we find more plasticity: ionocytes are more frequently restricted to the filament in SW, but also spread to SL in FW. It may be that the occurrence of ionocytes in SL is the ancestral condition, but some euryhaline acanthopterygians rely on the space of the SL for placement of additional ionocytes when in FW absorbing salt. Our study contributed to the identification of the pattern of ionocyte distribution in gills of Ostariophysi in respect to that of Acanthopterygii.

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Data availability

Data can be made available on request to Dr. Carolina A. Freire.

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Acknowledgements

This work is part of the Doctoral Dissertation of FJMC, conducted at the Graduate Program in Physiology of the Federal University of Paraná (UFPR) (http://hdl.handle.net/1884/28411). The authors also wish to thank the help by Professor Edvaldo S. Trindade, as well as from the technicians of the Confocal Microscopy Center of UFPR, Israel H. Bini, Lisandra S. Ferreira-Maba, and Alessandra C. S. dos Santos. The authors also thank the Hybridoma Bank of the Department of Biological Sciences of the University of Iowa, for the production of the antibody to the NKA. The authors also thank both reviewers for very useful suggestions to improve the manuscript.

Funding

This study received financing from CNPq (Research Grants awarded to CAF, #306630/2011–7, and #479350/2010–8), and CAPES-PRODOC (AUXPE PRODOC 2620/2010), Brazilian Government Sponsors.

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Contributions

CAF had the original idea and FJMC and VP prepared the samples and produced the images and discussed the data; FJMC wrote a first version of the manuscript. CAF prepared the table with FJMC and VP and organized the analysis and discussion of the results and edited the text of the manuscript to its final form.

Corresponding author

Correspondence to Carolina A. Freire.

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Ethics approval

Experimental handling of the fish was approved by the Ethics Committee on Animal Research of the Biological Sciences Sector of the Federal University of Paraná (CEUA Certificate #550, issued on June 7, 2011).

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The authors declare no competing interests.

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Highlights

• The distribution of Na+/K+-ATPase (NKA) immunoreactive ionocytes has been compared between two superorders;

• NKA was immunodetected in the filament and secondary lamellae in the four Ostariophysii;

• NKA ionocytes were restricted to the filaments in the three Acanthopterygii, in species from both freshwater and seawater;

• Lamellar ionocytes are more frequent in the gills of primary freshwater fishes, or euryhaline fishes acclimated to FW.

Supplementary Information

Table S1

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Ceron, F.J.M., Prodocimo, V. & Freire, C.A. Distribution of Na+/K+-ATPase-immunoreactive ionocytes varies between two superorders of ray-finned fish: Ostariophysi and Acanthopterygii. Fish Physiol Biochem 47, 1063–1071 (2021). https://doi.org/10.1007/s10695-021-00963-4

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  • DOI: https://doi.org/10.1007/s10695-021-00963-4

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