Distinct pathways for zinc metabolism in the terrestrial slug Arion vulgaris

Martin Dvorak,Willy Salvenmoser,Herbert Lindner,Markus Leiminger,Òscar Palacios,Oliver Zerbe,Armin Hansel,Reinhard Lackner,Raimund Schnegg,Gerhard Steiner,Reinhard Dallinger

doi:10.1038/s41598-019-56577-7

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+.

Highlights

In most organisms, the concentration of free Zn2+ is controlled by metallothioneins (MTs)
The overall picture is that vertebrate MTs are considered to be largely unspecific and ready to scavenge in their two metal binding domains different metal ions like Cu+, Cd2+, Zn2+, and many others, simultaneously[5]
As previously shown for Cd and Cu4, Zn is predominantly accumulated in the midgut gland of Arion vulgaris (Fig. 1)

Summary

Introduction

The concentration of free Zn2+ is controlled by metallothioneins (MTs). Metallothioneins (MTs) can bind transition metal ions with high affinity through the sulphur atoms of their cysteine residues They are known to play a crucial role in regulation, inactivation and metabolism of trace elements[3,4]. Such a metabolic separation of Zn2+ pathways is suggested by the fact that upon gel chromatography of midgut gland extracts from Arion vulgaris, the Cd-containing fractions assigned to MT are clearly separated from the Zn-containing fractions which elute at a much lower molecular weight This suggest that in invertebrates like Arion vulgaris, there may be specific pathways for different metal ions and indicate that the expression of cadmium selective MTs requires the presence of more specific pathways for other metal ions like Zn2+. Our conclusion is that in animals with highly metal-selective MTs for discrimination of Cd2+ and/or Cu+ -specific pathways (like in terrestrial snails), even more specific mechanisms are needed for handling of other metals such as the essential trace element Zn2+

Methods

Results

Conclusion