Abstract

Euryhaline teleosts exhibit major changes in renal function as they move between freshwater (FW) and seawater (SW) environments, thus tolerating large fluctuations in salinity. In FW, the kidney excretes large volumes of water through high glomerular filtration rates (GFR) and low tubular reabsorption rates, while actively reabsorbing most ions at high rates. The excreted product has a high urine flow rate (UFR) with a dilute composition. In SW, GFR is greatly reduced, and the tubules reabsorb as much water as possible, while actively secreting divalent ions. The excreted product has a low UFR, and is almost isosmotic to the blood plasma, with Mg2+, SO42–, and Cl– as the major ionic components. Early studies at the organismal level have described these basic patterns, while in the last two decades, studies of regulation at the cell and molecular level have been implemented, though only in a few euryhaline groups (salmonids, eels, tilapias, and fugus). There have been few studies combining the two approaches. The aim of the review is to integrate known aspects of renal physiology (reabsorption and secretion) with more recent advances in molecular water and solute physiology (gene and protein function of transporters). The renal transporters addressed include the subunits of the Na+, K+- ATPase (NKA) enzyme, monovalent ion transporters for Na+, Cl–, and K+ (NKCC1, NKCC2, CLC-K, NCC, ROMK2), water transport pathways [aquaporins (AQP), claudins (CLDN)], and divalent ion transporters for SO42–, Mg2+, and Ca2+ (SLC26A6, SLC26A1, SLC13A1, SLC41A1, CNNM2, CNNM3, NCX1, NCX2, PMCA). For each transport category, we address the current understanding at the molecular level, try to synthesize it with classical knowledge of overall renal function, and highlight knowledge gaps. Future research on the kidney of euryhaline fishes should focus on integrating changes in kidney reabsorption and secretion of ions with changes in transporter function at the cellular and molecular level (gene and protein verification) in different regions of the nephrons. An increased focus on the kidney individually and its functional integration with the other osmoregulatory organs (gills, skin and intestine) in maintaining overall homeostasis will have applied relevance for aquaculture.

Highlights

  • Several teleost fish species have developed strategies to maintain fluid and electrolyte homeostasis in a wide range of salinities, involving integrated ion and water transport activities of the gills, kidney and intestine (Evans et al, 2005; Marshall and Grosell, 2005; Evans, 2010; Grosell, 2010)

  • Urine concentrations of SO42− have been used as a marker for renal failure in humans, the transport pathways have been widely examined in the mammalian kidney (Markovich, 2001; Dawson et al, 2003; Markovich and Aronson, 2007)

  • FW teleosts actively take up SO42− from the environment, whereas in SW, there is an unavoidable influx of SO42− through the gills, and perhaps slight uptake in the gut: 97% of the excess SO42− is excreted through the kidney (Watanabe and Takei, 2012)

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Summary

INTRODUCTION

Several teleost fish species have developed strategies to maintain fluid and electrolyte homeostasis in a wide range of salinities, involving integrated ion and water transport activities of the gills, kidney and intestine (Evans et al, 2005; Marshall and Grosell, 2005; Evans, 2010; Grosell, 2010). The plasticity originating from the teleosts specific WGD3 events approximately 320350 million years ago (mya) and salmoniformes WGD4 events 50-80 mya may have enhanced the capacities for euryhaline species in these phyla to deal with salinity fluctuations and to acclimate to FW and SW environments (Houston and Macqueen, 2019) In their seminal review, Hickman and Trump (1969) provided a detailed overview of the evolution and anatomy of the teleost kidney. All parts of the nephron tubules and urinary bladder exhibit transport processes that contribute to the final volume and composition of the urine

RENAL HANDLING OF IONS AND WATER IN FW AND SW ENVIRONMENTS
Other Important Renal Monovalent Ion Transporters
Summary and Knowledge Gaps in Monovalent Ion Transport of the Kidney
Summary of AQPs and Their Relation to Ion Transport
FUTURE RESEARCH DIRECTIONS
Expression Profiling Along the Nephron
Findings
Comparative Studies on Mammals and Teleosts
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