Fooling a freshwater fish: how dietary salt transforms the rainbow trout gill into a seawater gill phenotype

Perry, Steve F.; Rivero-Lopez, Luis; McNeill, Brian; Wilson, Jonathan M.

doi:10.1242/jeb.02558

Cited by 41 publications

(28 citation statements)

References 27 publications

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“…Values are determined from three ranges of blood volume manipulation: 90 -100 -110%, 80 -90 -100%, and 100 -110 -120%. * †Significantly different from respective freshwater control, P Յ 0.05. may (5) or may not (18, 28; this study) return to prefeeding levels within 24 -48 h, there are physiological responses, such as net sodium efflux (34), increased drinking (28), and changes in gill morphology and enzymes (27,32), that are consistent with salt-loaded SW trout. However, unlike SW trout, urinary water loss is increased in FW-HS trout (31), consistent with a concomitant volume overload, which was also reflected in the increased blood volume of FW-HS trout (Table 1).…”

Section: Discussionmentioning

confidence: 85%

Effects of freshwater and saltwater adaptation and dietary salt on fluid compartments, blood pressure, and venous capacitance in trout

Olson¹,

Hoagland²

2008

American Journal of Physiology-Regulatory, Integrative and Comp

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Olson KR, Hoagland TM. Effects of freshwater and saltwater adaptation and dietary salt on fluid compartments, blood pressure, and venous capacitance in trout. Am J Physiol Regul Integr Comp Physiol 294: R1061-R1067, 2008. First published January 9, 2008 doi:10.1152/ajpregu.00698.2007.-Trout are of interest in defining the relationship between fluid and salt balance on cardiovascular function because they thrive in freshwater (FW; volume loading, salt depleting), saltwater (SW; volume depleting, salt loading), and FW while fed a high-salt diet (FW-HS; volume and salt loading). The effects of chronic (Ͼ2 wk) adaptation to these three protocols on blood volume ( 51 Cr red cell space), extracellular fluid volume ( 99m Tc-diethylene triaminepenta-acetic acid space), arterial (dorsal aortic; PDA) and venous (ductus Cuvier; Pven) blood pressure, mean circulatory filling pressure (zero-flow Pven), and vascular capacitance were examined in the present study on unanesthetized rainbow trout. Blood volume, extracellular fluid volume, PDA, Pven, and mean circulatory filling pressure progressively increased in the order SW Ͻ FW Ͻ FW-HS. Vascular capacitance in SW fish appeared to be continuous with the capacitance curve of FW fish and reflect a passive volume-dependent unloading of the venous system of FW fish. Vascular capacitance curves for FW-HS fish were displaced upward and parallel to those of FW fish, indicative of an active increase in unstressed blood volume without any change in vascular compliance. These studies are the first in any vertebrate to measure the relationship between fluid compartments and cardiovascular function during independent manipulation of volume and salt balance, and they show that volume, but not salt, balance is the primary determinant of blood pressure in trout. They also present a new paradigm with which to investigate the relative contributions of water and salt balance in cardiovascular homeostasis. fish; unstressed blood volume; mean circulatory filling pressure; osmoregulation; ionoregulation THE PIONEERING STUDIES OF Goldblatt et al. (13), Guyton et al. (15), Dahl and Heine (8), and others clearly showed that salt and water balance were primary effectors of blood pressure in mammals. Although a direct effect of salt balance on blood pressure has been suggested (2), it is generally accepted that fluid volume is the primary effector of blood pressure and that salt balance is regulated to maintain fluid volume. This is not surprising, as water loss in the urine or through evaporation is a chronic problem for terrestrial vertebrates, and, because water is not actively transported, it can only be retained if osmotically coupled to an osmolyte, usually salt. However, the inexorable coupling of water and salt has been problematic in understanding the pathophysiology of blood pressure regulation (2, 19, 35).The relative impact of volume regulation and salt balance on blood pressure regulation in fish may be more amenable to experimentation. Saltwater (SW) fish live in an environment with a ...

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Section: Discussionmentioning

confidence: 85%

Effects of freshwater and saltwater adaptation and dietary salt on fluid compartments, blood pressure, and venous capacitance in trout

Olson¹,

Hoagland²

2008

American Journal of Physiology-Regulatory, Integrative and Comp

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show abstract

“…Based on the limited available studies, this seems to indeed be the case (Chen et al, 2007;Olson and Hoagland, 2008;Perry et al, 2006). The adaptation from FW to SW results in a significantly elevated plasma osmolarity, and has been reported to produce a significantly lower dorsal aortic pressure (P DA ), central venous pressure (P VEN ) and mean circulatory filling pressure (MCFP) largely via a reduction in blood volume.…”

Section: Discussionmentioning

confidence: 97%

The response of non-traditional natriuretic peptide production sites to salt and water manipulations in the rainbow trout

Johnson

Olson

2009

Journal of Experimental Biology

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SUMMARYNatriuretic peptides (NPs) and their receptors (NPRs) comprise an evolutionarily conserved signaling system with profound physiological effects on vertebrate renal and cardiovascular systems. Some NPs (ANP, BNP and VNP) are primarily of cardiac origin whereas CNP is common in the brain. In mammals, non-traditional sites of NPs synthesis, BNP in brain and CNP in atrium, appear to have complementary actions. In the present study, trout were chronically adapted to freshwater (FW) (a volume-loading, salt-depleting environment), saltwater (SW) (a volume-depleting, salt-loading environment), FW and fed a high-salt diet (FW-HSD) (a volume-and salt-loading regime) or acutely volume depleted or expanded by hemorrhage or infusion with dialyzed plasma to perturb volume homeostasis. The responses of brain and atrial BNP and CNP mRNA, pro-peptide, NPR-A and NPR-B were evaluated using quantitative PCR and western analysis. Brain pro-BNP and NPR-A was increased in FW-HSD trout and decreased in SW trout. Brain pro-CNP was largely unaffected whereas NPR-B mRNA was increased in FW-HSD trout. Atrial CNP, although produced at lower levels than other cardiac NPs, was markedly elevated in chronically (FW-HSD) and acutely volume expanded trout (dialyzed-plasma infusion) whereas decreased in hemorrhaged trout. These findings indicate that non-traditional NP synthesis sites in the trout probably complement the broad hypovolemic and hypotensive actions of traditional (cardiac) NP synthesis sites in response to volume expansion but not to plasma osmolarity. This supports the hypothesis that the piscine and mammalian NP systems are fundamentally similar and appear to protect the heart from volume overload.

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“…There are several possible explanations for the presence of NKCC in the gill of freshwater salmonids. NKCC may be present to provide as minimal level of salt secretory capability in the event of encountering salt water or a high salt item in the diet (Perry et al, 2006). Alternatively, the presence of NKCC immunoreactivity in MRCs in freshwater may indicate that this transporter has some direct physiological function in ion uptake, or is involved in cell volume or acid/base regulation.…”

Section: Discussionmentioning

confidence: 99%

Variation in salinity tolerance, gill Na+/K+-ATPase,Na+/K+/2Cl– cotransporter and mitochondria-rich cell distribution in three salmonids Salvelinus namaycush, Salvelinus fontinalis and Salmo salar

Hiroi

McCormick

2007

Journal of Experimental Biology

110

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SUMMARY We compared seawater tolerance, gill Na+/K+-ATPase and Na+/K+/2Cl– cotransporter (NKCC)abundance, and mitochondria-rich cell (MRC) morphology of three salmonids,lake trout Salvelinus namaycush, brook trout Salvelinus fontinalis and Atlantic salmon Salmo salar. They were transferred directly from 0 p.p.t. (parts per thousand; freshwater) to 30 p.p.t. seawater, or transferred gradually from 0 to 10, 20 and 30 p.p.t. at 1-week intervals and kept in 30 p.p.t. for 3 weeks. The survival rates of lake trout, brook trout and Atlantic salmon were 80%, 50% and 100% following direct transfer, and 80%, 100% and 100% during gradual transfer, respectively. Plasma Na+, K+ and Cl– concentrations in surviving lake trout increased rapidly and remained at high levels in 30 p.p.t. of both direct and gradual transfer, whereas those in brook trout showed a transient increase following direct transfer but did not change significantly during gradual transfer. Only minor changes in plasma ions were observed in Atlantic salmon smolts in both direct and gradual transfer. These results suggest that lake trout retains some degree of euryhalinity and that brook trout possesses intermediate euryhalinity between lake trout and Atlantic salmon smolts. Gill Na+/K+-ATPase activity of lake trout and brook trout increased in seawater, whereas that of Atlantic salmon smolts was already upregulated in freshwater and remained high after seawater exposure. NKCC abundance was upregulated in parallel with gill Na+/K+-ATPase activity in each species. Immunocytochemistry with anti-Na+/K+-ATPaseα-subunit and anti-NKCC revealed that the two ion transporters were colocalized on the basolateral membrane of gill MRCs. Immunopositive MRCs were distributed on both primary filaments and secondary lamellae in all three species kept in freshwater; following transfer to seawater this pattern did not change in lake trout and brook trout but lamellar MRCs disappeared in Atlantic salmon. Previous studies on several teleost species have suggested that filament and lamellar MRCs would be involved in seawater and freshwater acclimation, respectively. However, our results in lake trout and brook trout suggest that lamellar MRCs could be also functional during seawater acclimation.

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Fooling a freshwater fish: how dietary salt transforms the rainbow trout gill into a seawater gill phenotype

Cited by 41 publications

References 27 publications

Effects of freshwater and saltwater adaptation and dietary salt on fluid compartments, blood pressure, and venous capacitance in trout

Effects of freshwater and saltwater adaptation and dietary salt on fluid compartments, blood pressure, and venous capacitance in trout

The response of non-traditional natriuretic peptide production sites to salt and water manipulations in the rainbow trout

Variation in salinity tolerance, gill Na+/K+-ATPase,Na+/K+/2Cl– cotransporter and mitochondria-rich cell distribution in three salmonids Salvelinus namaycush, Salvelinus fontinalis and Salmo salar

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