Distinct pathways for zinc metabolism in the terrestrial slug Arion vulgaris

Abstract In most organisms, the concentration of free Zn2+ is controlled by metallothioneins (MTs). In contrast, no significant proportions of Zn2+ are bound to MTs in the slug, Arion vulgaris. Instead, this species possesses cytoplasmic low-molecular-weight Zn2+ (LMW Zn) binding compound that diver...

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Main Authors: Martin Dvorak, Raimund Schnegg, Willy Salvenmoser, Òscar Palacios, Herbert Lindner, Oliver Zerbe, Armin Hansel, Markus Leiminger, Gerhard Steiner, Reinhard Dallinger, Reinhard Lackner
Format: Article
Language:English
Published: Nature Publishing Group 2019-12-01
Series:Scientific Reports
Online Access:https://doi.org/10.1038/s41598-019-56577-7
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spelling doaj-a9e6dc91279141f198376b3b970fe2902020-12-27T12:11:42ZengNature Publishing GroupScientific Reports2045-23222019-12-019111010.1038/s41598-019-56577-7Distinct pathways for zinc metabolism in the terrestrial slug Arion vulgarisMartin Dvorak0Raimund Schnegg1Willy Salvenmoser2Òscar Palacios3Herbert Lindner4Oliver Zerbe5Armin Hansel6Markus Leiminger7Gerhard Steiner8Reinhard Dallinger9Reinhard Lackner10Institute of Zoology and Center of Molecular Biosciences, University of InnsbruckInstitute of Zoology and Center of Molecular Biosciences, University of InnsbruckInstitute of Zoology and Center of Molecular Biosciences, University of InnsbruckDepartament de Química, Facultat de Ciències, Universitat Autònoma de BarcelonaInstitute of Clinical Biochemistry, Biocenter, Innsbruck Medical UniversityDepartment of Chemistry, University of ZurichInstitute for Ion Physics and Applied Physics, University of InnsbruckInstitute for Ion Physics and Applied Physics, University of InnsbruckInstitute for Ion Physics and Applied Physics, University of InnsbruckInstitute of Zoology and Center of Molecular Biosciences, University of InnsbruckInstitute of Zoology and Center of Molecular Biosciences, University of InnsbruckAbstract In most organisms, the concentration of free Zn2+ is controlled by metallothioneins (MTs). In contrast, no significant proportions of Zn2+ are bound to MTs in the slug, Arion vulgaris. Instead, this species possesses cytoplasmic low-molecular-weight Zn2+ (LMW Zn) binding compound that divert these metal ions into pathways uncoupled from MT metabolism. Zn2+ is accumulated in the midgut gland calcium cells of Arion vulgaris, where they associate with a low-molecular-weight ligand with an apparent molecular mass of ~ 2,000 Da. Mass spectrometry of the semi-purified LMW Zn binding compound combining an electrospray ion source with a differential mobility analyser coupled to a time-of-flight mass spectrometer revealed the presence of four Zn2+-containing ion signals, which arise from disintegration of one higher MW complex resulting in an ion-mobility diameter of 1.62 nm and a molecular mass of 837 Da. We expect that the novel Zn2+ ion storage pathway may be shared by many other gastropods, and particularly species that possess Cd-selective MT isoforms or variants with only very low affinity to Zn2+.https://doi.org/10.1038/s41598-019-56577-7
collection DOAJ
language English
format Article
sources DOAJ
author Martin Dvorak
Raimund Schnegg
Willy Salvenmoser
Òscar Palacios
Herbert Lindner
Oliver Zerbe
Armin Hansel
Markus Leiminger
Gerhard Steiner
Reinhard Dallinger
Reinhard Lackner
spellingShingle Martin Dvorak
Raimund Schnegg
Willy Salvenmoser
Òscar Palacios
Herbert Lindner
Oliver Zerbe
Armin Hansel
Markus Leiminger
Gerhard Steiner
Reinhard Dallinger
Reinhard Lackner
Distinct pathways for zinc metabolism in the terrestrial slug Arion vulgaris
Scientific Reports
author_facet Martin Dvorak
Raimund Schnegg
Willy Salvenmoser
Òscar Palacios
Herbert Lindner
Oliver Zerbe
Armin Hansel
Markus Leiminger
Gerhard Steiner
Reinhard Dallinger
Reinhard Lackner
author_sort Martin Dvorak
title Distinct pathways for zinc metabolism in the terrestrial slug Arion vulgaris
title_short Distinct pathways for zinc metabolism in the terrestrial slug Arion vulgaris
title_full Distinct pathways for zinc metabolism in the terrestrial slug Arion vulgaris
title_fullStr Distinct pathways for zinc metabolism in the terrestrial slug Arion vulgaris
title_full_unstemmed Distinct pathways for zinc metabolism in the terrestrial slug Arion vulgaris
title_sort distinct pathways for zinc metabolism in the terrestrial slug arion vulgaris
publisher Nature Publishing Group
series Scientific Reports
issn 2045-2322
publishDate 2019-12-01
description Abstract In most organisms, the concentration of free Zn2+ is controlled by metallothioneins (MTs). In contrast, no significant proportions of Zn2+ are bound to MTs in the slug, Arion vulgaris. Instead, this species possesses cytoplasmic low-molecular-weight Zn2+ (LMW Zn) binding compound that divert these metal ions into pathways uncoupled from MT metabolism. Zn2+ is accumulated in the midgut gland calcium cells of Arion vulgaris, where they associate with a low-molecular-weight ligand with an apparent molecular mass of ~ 2,000 Da. Mass spectrometry of the semi-purified LMW Zn binding compound combining an electrospray ion source with a differential mobility analyser coupled to a time-of-flight mass spectrometer revealed the presence of four Zn2+-containing ion signals, which arise from disintegration of one higher MW complex resulting in an ion-mobility diameter of 1.62 nm and a molecular mass of 837 Da. We expect that the novel Zn2+ ion storage pathway may be shared by many other gastropods, and particularly species that possess Cd-selective MT isoforms or variants with only very low affinity to Zn2+.
url https://doi.org/10.1038/s41598-019-56577-7
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