Metallothioneins of the urochordate<i>Oikopleura dioica</i>have Cys-rich tandem repeats, large size and cadmium-binding preference

Calatayud, Sara; Garcia-Risco, Mario; Rojas, Natalia S; Espinosa-Sánchez, Lizethe; Artime, Sebastián; Palacios, Òscar; Cañestro, Cristian; Albalat, Ricard

doi:10.1039/c8mt00177d

Cited by 14 publications

(32 citation statements)

References 74 publications

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“…The arrangement of Cys motifs in O. dioica domains diverges from that found in the MTs of other tunicates belonging to the ascidian and thaliacean classes, but it is similar to that of other appendicularian species of the same genus, O. albicans and O. vanhoeffeni (Calatayud et al, 2021a). Comparison of the appendicularian MTs show that the original Oikopleura MT domain had twelve cysteines (12C), and that this domain corresponds to previously described C7 + C5 subunits (Calatayud et al, 2018(Calatayud et al, , 2021a. OdiMT1 would have therefore two 12C domains, but its amino-terminal domain was "trimmed" to become a t-12C domain that lacks the C5 subunit.…”

Section: Introductionmentioning

confidence: 48%

“…O. dioica has two MTs, a bi-modular OdiMT1 and a multimodular OdiMT2 (formerly OdMT1 and OdMT2) made of different number of domain repeats (Calatayud et al, 2018). The arrangement of Cys motifs in O. dioica domains diverges from that found in the MTs of other tunicates belonging to the ascidian and thaliacean classes, but it is similar to that of other appendicularian species of the same genus, O. albicans and O. vanhoeffeni (Calatayud et al, 2021a).…”

Section: Introductionmentioning

confidence: 94%

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Modular Evolution and Population Variability of Oikopleura dioica Metallothioneins

Calatayud

Garcia-Risco

Capdevila

et al. 2021

Front. Cell Dev. Biol.

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Chordate Oikopleura dioica probably is the fastest evolving metazoan reported so far, and thereby, a suitable system in which to explore the limits of evolutionary processes. For this reason, and in order to gain new insights on the evolution of protein modularity, we have investigated the organization, function and evolution of multi-modular metallothionein (MT) proteins in O. dioica. MTs are a heterogeneous group of modular proteins defined by their cysteine (C)-rich domains, which confer the capacity of coordinating different transition metal ions. O. dioica has two MTs, a bi-modular OdiMT1 consisting of two domains (t-12C and 12C), and a multi-modular OdiMT2 with six t-12C/12C repeats. By means of mass spectrometry and spectroscopy of metal-protein complexes, we have shown that the 12C domain is able to autonomously bind four divalent metal ions, although the t-12C/12C pair –as it is found in OdiMT1– is the optimized unit for divalent metal binding. We have also shown a direct relationship between the number of the t-12C/12C repeats and the metal-binding capacity of the MTs, which means a stepwise mode of functional and structural evolution for OdiMT2. Finally, after analyzing four different O. dioica populations worldwide distributed, we have detected several OdiMT2 variants with changes in their number of t-12C/12C domain repeats. This finding reveals that the number of repeats fluctuates between current O. dioica populations, which provides a new perspective on the evolution of domain repeat proteins.

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Section: Introductionmentioning

confidence: 48%

Section: Introductionmentioning

confidence: 94%

Modular Evolution and Population Variability of Oikopleura dioica Metallothioneins

Calatayud

Garcia-Risco

Capdevila

et al. 2021

Front. Cell Dev. Biol.

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“…Intron loss can be a sign for pseudogenization [46], meaning that the respective gene is not transcribed into mRNA any more, which normally serves as a template for translation into the respective protein. [47]; H.p., Helix pomatia [13]; B.g., Biomphalaria glabrata [48]; A.b., Alinda biplicata (this study); T.m., Tremella mesenterica [49]; C.v., Crassostrea virginica [50]; T.p., Tetrahymena pyriformis [51].…”

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

confidence: 99%

“…All these features argue against the pseudogenization of the two intronless MT genes. Overall, the internal architecture of MT genes can be very variable ( Figure 3), and three different kinds of MT gene structures can be distinguished: (i) a typical exon/intron structure as known for many other genes, too [13,[47][48][49][50]; (ii) a deviated exon/intron structure with a large exon consisting of repeat sequences that sometimes represent multiple domains [47]; and (iii) real intronless genes where introns are not present anymore [51] (this study). In addition, the length of the introns can vary to a great extent, mostly in contrast to the rather uniform size of exons ( Figure 3).…”

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

confidence: 99%

“…The 10md-MT gene of A. biplicata encodes a putative md-MT protein with 319 aas, thus being the longest MT ever so far described from a mollusk species. Only for the sea squirt Oikopleura dioica a longer MT variant with 399 aas was reported [47]. In addition to the 10md-MT, A. biplicata possesses a second large-sized md-MT isoform with 287 aas, encoded by the 9md-MT gene (Figures 4 and 6).…”

Section: Are Alinda Biplicata Md-mts Involved In CD Detoxification?mentioning

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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Oikopleura dioica: An Emergent Chordate Model to Study the Impact of Gene Loss on the Evolution of the Mechanisms of Development

Ferrández-Roldán

Martí-Solans

Cañestro

et al. 2019

Results and Problems in Cell Differentiation

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The urochordate Oikopleura dioica is emerging as a nonclassical animal model in the field of evolutionary developmental biology (a.k.a. evo-devo) especially attractive for investigating the impact of gene loss on the evolution of mechanisms of development. This is because this organism fulfills the requirements of an animal model (i.e., has a simple and accessible morphology, a short generation time and life span, and affordable culture in the laboratory and amenable experimental manipulation), but also because O. dioica occupies a key phylogenetic position to understand the diversification and origin of our own phylum, the chordates. During its evolution, O. dioica genome has suffered a drastic process of compaction, becoming the smallest known chordate genome, a process that has been accompanied by exacerbating amount of gene losses. Interestingly, however, despite the extensive gene losses, including entire regulatory pathways essential for the embryonic development of other chordates, O. dioica retains the typical chordate body plan. This unexpected situation led to the formulation of the so-called inverse paradox of evo-devo, that is, when a genetic diversity is able to maintain a phenotypic unity. This chapter reviews the biological features of O. dioica as a model animal, along with the current data on the evolution of its genes and genome. We pay special attention to the numerous examples of gene losses that have taken place during the evolution of this unique animal model, which is helping us to understand to which the limits of evo-devo can be pushed off.

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Metallothioneins of the urochordateOikopleura dioicahave Cys-rich tandem repeats, large size and cadmium-binding preference

Abstract: Oikopleura dioica has the longest metallothionein described so far, made of repeats generated by a modular and step-wise evolution.

Cited by 14 publications

References 74 publications

Modular Evolution and Population Variability of Oikopleura dioica Metallothioneins

Modular Evolution and Population Variability of Oikopleura dioica Metallothioneins

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

Oikopleura dioica: An Emergent Chordate Model to Study the Impact of Gene Loss on the Evolution of the Mechanisms of Development

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