Metallomics reveals a persisting impact of cadmium on the evolution of metal-selective snail metallothioneins

Dallinger, Reinhard; Zerbe, Oliver; Baumann, Christian; Egger, Bernhard; Capdevila, Mercè; Palacios, Òscar; Albalat, Ricard; Calatayud, Sara; Ladurner, Peter; Schlick‐Steiner, Birgit C.; Steiner, Florian M.; Pedrini-Martha, Veronika; Lackner, Reinhard; Lindner, Herbert; Dvorak, Martin; Niederwanger, Michael; Schnegg, Raimund; Atrian, Sı́lvia

doi:10.1039/c9mt00259f

Cited by 16 publications

(65 citation statements)

References 89 publications

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“…At moderately increased Cd exposure concentrations in our study (Cd10 in Figure 5), MT genes (md-MTs and CuMT) of A. biplicata are upregulated with an approximately 3.5-fold induction ( Figure 5C), very probably in response to Cd stress in order to handle its detoxification. Such a rather moderate activation for MT gene expression due to Cd exposure was reported for other gastropod species, too, such as Helix pomatia or Cornu aspersum [14,19], where Cd 2+ ions are readily detoxified by binding to the produced CdMT proteins [6,72]. In contrast, Cd-dependent MT gene upregulation is much stronger in vertebrates like rats [73], fish [74][75][76], or other invertebrate species like in the earthworm Eisenia fetida [77].…”

Section: Impact Of CD Exposure On Mt Gene Transcription In Alinda Bipmentioning

confidence: 70%

“…Furthermore, both md-MT genes of A. biplicata are transcribed to RNA (Figure 4) [19]. Hence, due to the lack of introns, the DNA sequence of both md-MTs matches its respective RNA transcripts (Figure 4).…”

Section: Characterization Of Multi-domain Mt Genes In Alinda Biplicatamentioning

confidence: 99%

“…Apart from that, it has also been demonstrated that the C-terminal metal binding domains are highly conserved among all snail MTs. At least in the three-domain MT of Littorina littorea, the C-terminal domain has assumed an important role in cooperative uploading of Cd 2+ to the whole MT protein [19].…”

Section: Characterization Of Multi-domain Mt Genes In Alinda Biplicatamentioning

confidence: 99%

“…Consequently, these newly discovered three-domain MTs have increased their binding stoichiometry from 6 to 9 Cd 2+ ions [26,28]. Our most recent studies indicate the presence of multi-domain MTs (md-MTs) with as much as eight (8) metal-binding domains (8md-MT) in an MT of the freshwater snail Marisa cornuarietis, and with nine (9) or even ten (10) metal-binding domains (9md-MT and 10md-MT) in two MT isoforms of the terrestrial snail A. biplicata [19]. Following the findings of increased Cd-binding capacities in the three-domain MTs of Littorina littorea and Pomatias elegans (see above), we suggest that the additional multiplication of N-terminal metal-binding domains in the MTs of Marisa cornuarietis and A. biplicata might increase their metal ion stoichiometry and hence, their metal-binding capacity to a correspondingly high level.…”

Section: Introductionmentioning

confidence: 96%

“…Mono-and divalent metal ions such as Zn 2+ , Cd 2+ , or Cu + are bound by MTs through the sulfhydryl groups of cysteines arranged in highly conserved Cys-Xaa-Cys motifs, building firm metal thiolate clusters [17]. As a particular feature, many snail species express metal-selective MT variants and isoforms derived from metal-unspecific precursors in basal gastropod ancestors [18,19]. Metal-selective snail MTs were first discovered in the helicid snails Helix pomatia and Cornu aspersum.…”

Section: Introductionmentioning

confidence: 99%

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Cadmium Uptake, MT Gene Activation and Structure of Large-Sized Multi-Domain Metallothioneins in the Terrestrial Door Snail Alinda biplicata (Gastropoda, Clausiliidae)

Pedrini-Martha

Köll

Dvorak

et al. 2020

IJMS

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Terrestrial snails (Gastropoda) possess Cd-selective metallothioneins (CdMTs) that inactivate Cd2+ with high affinity. Most of these MTs are small Cysteine-rich proteins that bind 6 Cd2+ equivalents within two distinct metal-binding domains, with a binding stoichiometry of 3 Cd2+ ions per domain. Recently, unusually large, so-called multi-domain MTs (md-MTs) were discovered in the terrestrial door snail Alinda biplicata (A.b.). The aim of this study is to evaluate the ability of A.b. to cope with Cd stress and the potential involvement of md-MTs in its detoxification. Snails were exposed to increasing Cd concentrations, and Cd-tissue concentrations were quantified. The gene structure of two md-MTs (9md-MT and 10md-MT) was characterized, and the impact of Cd exposure on MT gene transcription was quantified via qRT PCR. A.b. efficiently accumulates Cd at moderately elevated concentrations in the feed, but avoids food uptake at excessively high Cd levels. The structure and expression of the long md-MT genes of A.b. were characterized. Although both genes are intronless, they are still transcribed, being significantly upregulated upon Cd exposure. Overall, our results contribute new knowledge regarding the metal handling of Alinda biplicata in particular, and the potential role of md-MTs in Cd detoxification of terrestrial snails, in general.

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Section: Impact Of CD Exposure On Mt Gene Transcription In Alinda Bipmentioning

confidence: 70%

Section: Characterization Of Multi-domain Mt Genes In Alinda Biplicatamentioning

confidence: 99%

Section: Characterization Of Multi-domain Mt Genes In Alinda Biplicatamentioning

confidence: 99%

Section: Introductionmentioning

confidence: 96%

Section: Introductionmentioning

confidence: 99%

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Cadmium Uptake, MT Gene Activation and Structure of Large-Sized Multi-Domain Metallothioneins in the Terrestrial Door Snail Alinda biplicata (Gastropoda, Clausiliidae)

Pedrini-Martha

Köll

Dvorak

et al. 2020

IJMS

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Responsiveness of metallothionein and hemocyanin genes to cadmium and copper exposure in the garden snail Cornu aspersum

et al. 2020

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Terrestrial gastropods express metal‐selective metallothioneins (MTs) by which they handle metal ions such as Zn2+, Cd2+, and Cu+/Cu2+ through separate metabolic pathways. At the same time, they depend on the availability of sufficient amounts of Cu as an essential constituent of their respiratory protein, hemocyanin (Hc). It was, therefore, suggested that in snails Cu‐dependent MT and Hc pathways might be metabolically connected. In fact, the Cu‐specific snail MT (CuMT) is exclusively expressed in rhogocytes, a particular molluscan cell type present in the hemocoel and connective tissues. Snail rhogocytes are also the sites of Hc synthesis. In the present study, possible interactions between the metal‐regulatory and detoxifying activity of MTs and the Cu demand of Hc isoforms was explored in the edible snail Cornu aspersum, one of the most common European helicid land snails. This species possesses CdMT and CuMT isoforms involved in metal‐selective physiological tasks. In addition, C. aspersum expresses three different Hc isoforms (CaH ɑD, CaH ɑN, CaH β). We have examined the effect of Cd2+ and Cu2+ exposure on metal accumulation in the midgut gland and mantle of C. aspersum, testing the impact of these metals on transcriptional upregulation of CdMT, CuMT, and the three Hc genes in the two organs. We found that the CuMT and CaH ɑD genes exhibit an organ‐specific transcriptional upregulation in the midgut gland of Cu‐exposed snails. These results are discussed in view of possible interrelationships between the metal‐selective activity of snail MT isoforms and the synthesis and metabolism of Hc isoforms.

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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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Metallomics reveals a persisting impact of cadmium on the evolution of metal-selective snail metallothioneins

Abstract: The tiny contribution of cadmium (Cd) to the composition of the earth's crust contrasts with its high biological significance. We suggest that in gastropod clades, the protein family of metallothioneins (MTs) has evolved to specifically detoxify Cd.

Cited by 16 publications

References 89 publications

Cadmium Uptake, MT Gene Activation and Structure of Large-Sized Multi-Domain Metallothioneins in the Terrestrial Door Snail Alinda biplicata (Gastropoda, Clausiliidae)

Cadmium Uptake, MT Gene Activation and Structure of Large-Sized Multi-Domain Metallothioneins in the Terrestrial Door Snail Alinda biplicata (Gastropoda, Clausiliidae)

Responsiveness of metallothionein and hemocyanin genes to cadmium and copper exposure in the garden snail Cornu aspersum

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

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