Effects of chronic waterborne nickel exposure on growth, ion homeostasis, acid-base balance, and nickel uptake in the freshwater pulmonate snail, Lymnaea stagnalis

Som Niyogi, Kevin V. Brix, Martin Grosell

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23 Citations (Scopus)

Abstract

The freshwater pulmonate snail, Lymnaea stagnalis, is the most sensitive aquatic organism tested to date for Ni. We undertook a series of experiments to investigate the underlying mechanism(s) for this observed hypersensitivity. Consistent with previous experiments, juvenile snail growth in a 21-day exposure was reduced by 48% relative to the control when exposed to 1.3μgl-1 Ni (EC20 less than the lowest concentration tested). Ca2+ homeostasis was significantly disrupted by Ni exposure as demonstrated by reductions in net Ca2+ uptake, and reductions in Ca2+ concentrations in the hemolymph and soft tissues. We also observed reduced soft tissue [Mg2+]. Snails underwent a significant alkalosis with hemolymph pH increasing from 8.1 to 8.3 and hemolymph TCO2 increasing from 19 to 22mM in control versus Ni-exposed snails, respectively. Unlike in previous studies with Co and Pb, snail feeding rates were found to be unaffected by Ni at the end of the exposure. Snails accumulated Ni in the soft tissue in a concentration-dependent manner, and Ni uptake experiments with 63Ni revealed a biphasic uptake profile - a saturable high affinity component at low exposure concentrations (36-189nM) and a linear component at the high exposure concentrations (189-1897nM). The high affinity transport system had an apparent Km of 89nM Ni2+ and Vmax of 2.4nmolg-1h-1. This equates to a logK of 7.1, significantly higher than logK's (2.6-5.2) for any other aquatic organisms evaluated to date, which will have implications for Biotic Ligand Model development. Finally, pharmacological inhibitors that block Ca2+ uptake pathways in snails did not inhibit Ni uptake, suggesting that the uptake of Ni does not occur via Ca2+ uptake pathways. As with Cu and Pb, the exact mechanism for the significant disruption in Ca2+ homeostasis and reduction in juvenile snail growth remains unknown.

Original languageEnglish
Pages (from-to)36-44
Number of pages9
JournalAquatic Toxicology
Volume150
DOIs
StatePublished - Jan 1 2014

Fingerprint

Lymnaea
Lymnaea stagnalis
acid-base balance
Acid-Base Equilibrium
Snails
homeostasis
Nickel
Fresh Water
nickel
snail
snails
long term effects
Homeostasis
Ions
ions
uptake mechanisms
ion
acid
Growth
calcium

Keywords

  • Chronic toxicity
  • Growth
  • Ion homeostasis
  • Nickel
  • Snail
  • Uptake kinetics

ASJC Scopus subject areas

  • Aquatic Science
  • Health, Toxicology and Mutagenesis

Cite this

@article{18cb30aa461f44628016a7c281b1a0a1,
title = "Effects of chronic waterborne nickel exposure on growth, ion homeostasis, acid-base balance, and nickel uptake in the freshwater pulmonate snail, Lymnaea stagnalis",
abstract = "The freshwater pulmonate snail, Lymnaea stagnalis, is the most sensitive aquatic organism tested to date for Ni. We undertook a series of experiments to investigate the underlying mechanism(s) for this observed hypersensitivity. Consistent with previous experiments, juvenile snail growth in a 21-day exposure was reduced by 48{\%} relative to the control when exposed to 1.3μgl-1 Ni (EC20 less than the lowest concentration tested). Ca2+ homeostasis was significantly disrupted by Ni exposure as demonstrated by reductions in net Ca2+ uptake, and reductions in Ca2+ concentrations in the hemolymph and soft tissues. We also observed reduced soft tissue [Mg2+]. Snails underwent a significant alkalosis with hemolymph pH increasing from 8.1 to 8.3 and hemolymph TCO2 increasing from 19 to 22mM in control versus Ni-exposed snails, respectively. Unlike in previous studies with Co and Pb, snail feeding rates were found to be unaffected by Ni at the end of the exposure. Snails accumulated Ni in the soft tissue in a concentration-dependent manner, and Ni uptake experiments with 63Ni revealed a biphasic uptake profile - a saturable high affinity component at low exposure concentrations (36-189nM) and a linear component at the high exposure concentrations (189-1897nM). The high affinity transport system had an apparent Km of 89nM Ni2+ and Vmax of 2.4nmolg-1h-1. This equates to a logK of 7.1, significantly higher than logK's (2.6-5.2) for any other aquatic organisms evaluated to date, which will have implications for Biotic Ligand Model development. Finally, pharmacological inhibitors that block Ca2+ uptake pathways in snails did not inhibit Ni uptake, suggesting that the uptake of Ni does not occur via Ca2+ uptake pathways. As with Cu and Pb, the exact mechanism for the significant disruption in Ca2+ homeostasis and reduction in juvenile snail growth remains unknown.",
keywords = "Chronic toxicity, Growth, Ion homeostasis, Nickel, Snail, Uptake kinetics",
author = "Som Niyogi and Brix, {Kevin V.} and Martin Grosell",
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T1 - Effects of chronic waterborne nickel exposure on growth, ion homeostasis, acid-base balance, and nickel uptake in the freshwater pulmonate snail, Lymnaea stagnalis

AU - Niyogi, Som

AU - Brix, Kevin V.

AU - Grosell, Martin

PY - 2014/1/1

Y1 - 2014/1/1

N2 - The freshwater pulmonate snail, Lymnaea stagnalis, is the most sensitive aquatic organism tested to date for Ni. We undertook a series of experiments to investigate the underlying mechanism(s) for this observed hypersensitivity. Consistent with previous experiments, juvenile snail growth in a 21-day exposure was reduced by 48% relative to the control when exposed to 1.3μgl-1 Ni (EC20 less than the lowest concentration tested). Ca2+ homeostasis was significantly disrupted by Ni exposure as demonstrated by reductions in net Ca2+ uptake, and reductions in Ca2+ concentrations in the hemolymph and soft tissues. We also observed reduced soft tissue [Mg2+]. Snails underwent a significant alkalosis with hemolymph pH increasing from 8.1 to 8.3 and hemolymph TCO2 increasing from 19 to 22mM in control versus Ni-exposed snails, respectively. Unlike in previous studies with Co and Pb, snail feeding rates were found to be unaffected by Ni at the end of the exposure. Snails accumulated Ni in the soft tissue in a concentration-dependent manner, and Ni uptake experiments with 63Ni revealed a biphasic uptake profile - a saturable high affinity component at low exposure concentrations (36-189nM) and a linear component at the high exposure concentrations (189-1897nM). The high affinity transport system had an apparent Km of 89nM Ni2+ and Vmax of 2.4nmolg-1h-1. This equates to a logK of 7.1, significantly higher than logK's (2.6-5.2) for any other aquatic organisms evaluated to date, which will have implications for Biotic Ligand Model development. Finally, pharmacological inhibitors that block Ca2+ uptake pathways in snails did not inhibit Ni uptake, suggesting that the uptake of Ni does not occur via Ca2+ uptake pathways. As with Cu and Pb, the exact mechanism for the significant disruption in Ca2+ homeostasis and reduction in juvenile snail growth remains unknown.

AB - The freshwater pulmonate snail, Lymnaea stagnalis, is the most sensitive aquatic organism tested to date for Ni. We undertook a series of experiments to investigate the underlying mechanism(s) for this observed hypersensitivity. Consistent with previous experiments, juvenile snail growth in a 21-day exposure was reduced by 48% relative to the control when exposed to 1.3μgl-1 Ni (EC20 less than the lowest concentration tested). Ca2+ homeostasis was significantly disrupted by Ni exposure as demonstrated by reductions in net Ca2+ uptake, and reductions in Ca2+ concentrations in the hemolymph and soft tissues. We also observed reduced soft tissue [Mg2+]. Snails underwent a significant alkalosis with hemolymph pH increasing from 8.1 to 8.3 and hemolymph TCO2 increasing from 19 to 22mM in control versus Ni-exposed snails, respectively. Unlike in previous studies with Co and Pb, snail feeding rates were found to be unaffected by Ni at the end of the exposure. Snails accumulated Ni in the soft tissue in a concentration-dependent manner, and Ni uptake experiments with 63Ni revealed a biphasic uptake profile - a saturable high affinity component at low exposure concentrations (36-189nM) and a linear component at the high exposure concentrations (189-1897nM). The high affinity transport system had an apparent Km of 89nM Ni2+ and Vmax of 2.4nmolg-1h-1. This equates to a logK of 7.1, significantly higher than logK's (2.6-5.2) for any other aquatic organisms evaluated to date, which will have implications for Biotic Ligand Model development. Finally, pharmacological inhibitors that block Ca2+ uptake pathways in snails did not inhibit Ni uptake, suggesting that the uptake of Ni does not occur via Ca2+ uptake pathways. As with Cu and Pb, the exact mechanism for the significant disruption in Ca2+ homeostasis and reduction in juvenile snail growth remains unknown.

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KW - Uptake kinetics

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