Metal binding functions of metallothioneins in the slug<i>Arion vulgaris</i>differ from metal-specific isoforms of terrestrial snails

Dvorak, Martin; Lackner, Reinhard; Niederwanger, Michael; Rotondo, Claire; Schnegg, Raimund; Ladurner, Peter; Pedrini-Martha, Veronika; Salvenmoser, Willi; Kremser, Leopold; Lindner, Herbert; Garcia-Risco, Mario; Calatayud, Sara; Albalat, Ricard; Palacios, Òscar; Capdevila, Mercè; Dallinger, Reinhard

doi:10.1039/c8mt00215k

Cited by 20 publications

(31 citation statements)

References 61 publications

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Section: Species-specific Differences In CD Uptake and The Role Of Mementioning

confidence: 53%

“…in Arion vulgaris and 3 µ g Cd/g in Biomphalaria glabrata, this corresponds to metal accumulation factors in the midgut gland of about 11 and 116, respectively. At the same time, no mortality was observed in the two species, confirming their high tolerance and detoxification capacity against this highly toxic metal [37,39]. In spite of the much stronger Cd accumulation in Biomphalaria glabrata, only in Arion vulgaris a significant transcriptional upregulation (9-fold) of the respective Cd-selective AvMT1 gene occurs (GenBank: MF155618, [39]).…”

Section: Species-specific Differences In CD Uptake and The Role Of Mementioning

confidence: 84%

“…At the same time, no mortality was observed in the two species, confirming their high tolerance and detoxification capacity against this highly toxic metal [37,39]. In spite of the much stronger Cd accumulation in Biomphalaria glabrata, only in Arion vulgaris a significant transcriptional upregulation (9-fold) of the respective Cd-selective AvMT1 gene occurs (GenBank: MF155618, [39]). In contrast, no detectable upregulation was observed for the unspecific MT gene of Biomphalaria glabrata (GenBank: KT697617, [37]) ( Figure 1B,C).…”

Section: Species-specific Differences In CD Uptake and The Role Of Mementioning

confidence: 84%

“…We compare two species of gastropods, Arion vulgaris and Biomphalaria glabrata, and their response to Cd exposure. Arion vulgaris possesses an inducible Cdselective MT (AvMT1) [39], while the second species relies on a non-selective MT that is hardly inducible by Cd exposure [37,40]. We provide evidence that in snails, PCs are ready to take over protection against Cd impact, if the detoxification capacity of MTs becomes deficient due to lacking metal binding selectivity or oversaturation of their binding capacity.…”

Section: Species-specific Differences In CD Uptake and The Role Of Mementioning

confidence: 92%

“…Since both species exhibit a considerable tolerance towards Cd upon metal exposure (see above), this suggests that the lacking inactivation capacity for Cd by the MT system in Biomphalaria glabrata must be compensated by an additional mechanism of detoxification. In spite of the much stronger Cd accumulation in Biomphalaria glabrata, only in Arion vulgaris a significant transcriptional upregulation (9-fold) of the respective Cd-selective AvMT1 gene occurs (GenBank: MF155618, [39]). In contrast, no detectable upregulation was observed for the unspecific MT gene of Biomphalaria glabrata (GenBank: KT697617, [37]) ( Figure 1B,C).…”

Section: Species-specific Differences In CD Uptake and The Role Of Mementioning

confidence: 99%

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Cadmium Pathways in Snails Follow a Complementary Strategy between Metallothionein Detoxification and Auxiliary Inactivation by Phytochelatins

Dvorak

Schnegg

Niederwanger

et al. 2019

IJMS

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Metal detoxification is crucial for animals to cope with environmental exposure. In snails, a pivotal role in protection against cadmium (Cd) is attributed to metallothioneins (MTs). Some gastropod species express, in a lineage-specific manner, Cd-selective MTs devoted exclusively to the binding and detoxification of this single metal, whereas other species of snails possess non-selective MTs, but still show a high tolerance against Cd. An explanation for this may be that invertebrates and in particular snails may also synthetize phytochelatins (PCs), originally known to be produced by plants, to provide protection against metal or metalloid toxicity. Here we demonstrate that despite the fact that similar mechanisms for Cd inactivation exist in snail species through binding of the metal to MTs, the actual detoxification pathways for this metal may follow different traits in a species-specific manner. In particular, this depends on the detoxification capacity of MTs due to their Cd-selective or non-specific binding features. In the terrestrial slug Arion vulgaris, for example, Cd is solely detoxified by a Cd-selective MT isoform (AvMT1). In contrast, the freshwater snail Biomphalaria glabrata activates an additional pathway for metal inactivation by synthesizing phytochelatins, which compensate for the insufficient capacity of its non-selective MT system to detoxify Cd. We hypothesize that in other snails and invertebrate species, too, an alternative inactivation of the metal by PCs may occur, if their MT system is not Cd-selective enough, or its Cd loading capacity is exhausted.

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Section: Species-specific Differences In CD Uptake and The Role Of Mementioning

confidence: 53%

Section: Species-specific Differences In CD Uptake and The Role Of Mementioning

confidence: 84%

Section: Species-specific Differences In CD Uptake and The Role Of Mementioning

confidence: 84%

Section: Species-specific Differences In CD Uptake and The Role Of Mementioning

confidence: 92%

Section: Species-specific Differences In CD Uptake and The Role Of Mementioning

confidence: 99%

See 3 more Smart Citations

Cadmium Pathways in Snails Follow a Complementary Strategy between Metallothionein Detoxification and Auxiliary Inactivation by Phytochelatins

Dvorak

Schnegg

Niederwanger

et al. 2019

IJMS

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Metals and metallothionein evolution in snails: a contribution to the concept of metal-specific functionality from an animal model group

Dallinger

2024

Biometals

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This is a critical review of what we know so far about the evolution of metallothioneins (MTs) in Gastropoda (snails, whelks, limpets and slugs), an important class of molluscs with over 90,000 known species. Particular attention will be paid to the evolution of snail MTs in relation to the role of some metallic trace elements (cadmium, zinc and copper) and their interaction with MTs, also compared to MTs from other animal phyla. The article also highlights the important distinction, yet close relationship, between the structural and metal-selective binding properties of gastropod MTs and their physiological functionality in the living organism. It appears that in the course of the evolution of Gastropoda, the trace metal cadmium (Cd) must have played an essential role in the development of Cd-selective MT variants. It is shown how the structures and Cd-selective binding properties in the basal gastropod clades have evolved by testing and optimizing different combinations of ancestral and novel MT domains, and how some of these domains have become established in modern and recent gastropod clades. In this context, the question of how adaptation to new habitats and lifestyles has affected the original MT traits in different gastropod lineages will also be addressed. The 3D structures and their metal binding preferences will be highlighted exemplarily in MTs of modern littorinid and helicid snails. Finally, the importance of the different metal requirements and pathways in snail tissues and cells for the shaping and functionality of the respective MT isoforms will be shown.

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Biological and biochemical assessment in Phorcus articulatus (Lamarck 1822): contamination and seasonal effect

Boulajfene

Strogyloudi

Lasram

et al. 2019

Environ Monit Assess

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Metal binding functions of metallothioneins in the slugArion vulgarisdiffer from metal-specific isoforms of terrestrial snails

Abstract: Arion vulgaris is a European slug with a huge potential for accumulating and detoxifying heavy metals.

Cited by 20 publications

References 61 publications

Cadmium Pathways in Snails Follow a Complementary Strategy between Metallothionein Detoxification and Auxiliary Inactivation by Phytochelatins

Cadmium Pathways in Snails Follow a Complementary Strategy between Metallothionein Detoxification and Auxiliary Inactivation by Phytochelatins

Metals and metallothionein evolution in snails: a contribution to the concept of metal-specific functionality from an animal model group

Biological and biochemical assessment in Phorcus articulatus (Lamarck 1822): contamination and seasonal effect

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