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Modular Evolution and Population Variability of Oikopleura dioica Metallothioneins

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 organizat...

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Autores principales: Calatayud, Sara, Garcia-Risco, Mario, Capdevila, Mercè, Cañestro, Cristian, Palacios, Òscar, Albalat, Ricard
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8283569/
https://www.ncbi.nlm.nih.gov/pubmed/34277643
http://dx.doi.org/10.3389/fcell.2021.702688
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author Calatayud, Sara
Garcia-Risco, Mario
Capdevila, Mercè
Cañestro, Cristian
Palacios, Òscar
Albalat, Ricard
author_facet Calatayud, Sara
Garcia-Risco, Mario
Capdevila, Mercè
Cañestro, Cristian
Palacios, Òscar
Albalat, Ricard
author_sort Calatayud, Sara
collection PubMed
description 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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spelling pubmed-82835692021-07-17 Modular Evolution and Population Variability of Oikopleura dioica Metallothioneins Calatayud, Sara Garcia-Risco, Mario Capdevila, Mercè Cañestro, Cristian Palacios, Òscar Albalat, Ricard Front Cell Dev Biol Cell and Developmental Biology 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. Frontiers Media S.A. 2021-07-02 /pmc/articles/PMC8283569/ /pubmed/34277643 http://dx.doi.org/10.3389/fcell.2021.702688 Text en Copyright © 2021 Calatayud, Garcia-Risco, Capdevila, Cañestro, Palacios and Albalat. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Cell and Developmental Biology
Calatayud, Sara
Garcia-Risco, Mario
Capdevila, Mercè
Cañestro, Cristian
Palacios, Òscar
Albalat, Ricard
Modular Evolution and Population Variability of Oikopleura dioica Metallothioneins
title Modular Evolution and Population Variability of Oikopleura dioica Metallothioneins
title_full Modular Evolution and Population Variability of Oikopleura dioica Metallothioneins
title_fullStr Modular Evolution and Population Variability of Oikopleura dioica Metallothioneins
title_full_unstemmed Modular Evolution and Population Variability of Oikopleura dioica Metallothioneins
title_short Modular Evolution and Population Variability of Oikopleura dioica Metallothioneins
title_sort modular evolution and population variability of oikopleura dioica metallothioneins
topic Cell and Developmental Biology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8283569/
https://www.ncbi.nlm.nih.gov/pubmed/34277643
http://dx.doi.org/10.3389/fcell.2021.702688
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