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Different skeletal protein toolkits achieve similar structure and performance in the tropical coral Stylophora pistillata and the temperate Oculina patagonica

Stony corals (order: Scleractinia) differ in growth form and structure. While stony corals have gained the ability to form their aragonite skeleton once in their evolution, the suite of proteins involved in skeletogenesis is different for different coral species. This led to the conclusion that the...

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Autores principales: Zaquin, Tal, Di Bisceglie, Anna Paola, Pinkas, Iddo, Falini, Giuseppe, Mass, Tali
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9532382/
https://www.ncbi.nlm.nih.gov/pubmed/36195656
http://dx.doi.org/10.1038/s41598-022-20744-0
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author Zaquin, Tal
Di Bisceglie, Anna Paola
Pinkas, Iddo
Falini, Giuseppe
Mass, Tali
author_facet Zaquin, Tal
Di Bisceglie, Anna Paola
Pinkas, Iddo
Falini, Giuseppe
Mass, Tali
author_sort Zaquin, Tal
collection PubMed
description Stony corals (order: Scleractinia) differ in growth form and structure. While stony corals have gained the ability to form their aragonite skeleton once in their evolution, the suite of proteins involved in skeletogenesis is different for different coral species. This led to the conclusion that the organic portion of their skeleton can undergo rapid evolutionary changes by independently evolving new biomineralization-related proteins. Here, we used liquid chromatography-tandem mass spectrometry to sequence skeletogenic proteins extracted from the encrusting temperate coral Oculina patagonica. We compare it to the previously published skeletal proteome of the branching subtropical corals Stylophora pistillata as both are regarded as highly resilient to environmental changes. We further characterized the skeletal organic matrix (OM) composition of both taxa and tested their effects on the mineral formation using a series of overgrowth experiments on calcite seeds. We found that each species utilizes a different set of proteins containing different amino acid compositions and achieve a different morphology modification capacity on calcite overgrowth. Our results further support the hypothesis that the different coral taxa utilize a species-specific protein set comprised of independent gene co-option to construct their own unique organic matrix framework. While the protein set differs between species, the specific predicted roles of the whole set appear to underline similar functional roles. They include assisting in forming the extracellular matrix, nucleation of the mineral and cell signaling. Nevertheless, the different composition might be the reason for the varying organization of the mineral growth in the presence of a particular skeletal OM, ultimately forming their distinct morphologies.
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spelling pubmed-95323822022-10-06 Different skeletal protein toolkits achieve similar structure and performance in the tropical coral Stylophora pistillata and the temperate Oculina patagonica Zaquin, Tal Di Bisceglie, Anna Paola Pinkas, Iddo Falini, Giuseppe Mass, Tali Sci Rep Article Stony corals (order: Scleractinia) differ in growth form and structure. While stony corals have gained the ability to form their aragonite skeleton once in their evolution, the suite of proteins involved in skeletogenesis is different for different coral species. This led to the conclusion that the organic portion of their skeleton can undergo rapid evolutionary changes by independently evolving new biomineralization-related proteins. Here, we used liquid chromatography-tandem mass spectrometry to sequence skeletogenic proteins extracted from the encrusting temperate coral Oculina patagonica. We compare it to the previously published skeletal proteome of the branching subtropical corals Stylophora pistillata as both are regarded as highly resilient to environmental changes. We further characterized the skeletal organic matrix (OM) composition of both taxa and tested their effects on the mineral formation using a series of overgrowth experiments on calcite seeds. We found that each species utilizes a different set of proteins containing different amino acid compositions and achieve a different morphology modification capacity on calcite overgrowth. Our results further support the hypothesis that the different coral taxa utilize a species-specific protein set comprised of independent gene co-option to construct their own unique organic matrix framework. While the protein set differs between species, the specific predicted roles of the whole set appear to underline similar functional roles. They include assisting in forming the extracellular matrix, nucleation of the mineral and cell signaling. Nevertheless, the different composition might be the reason for the varying organization of the mineral growth in the presence of a particular skeletal OM, ultimately forming their distinct morphologies. Nature Publishing Group UK 2022-10-04 /pmc/articles/PMC9532382/ /pubmed/36195656 http://dx.doi.org/10.1038/s41598-022-20744-0 Text en © The Author(s) 2022 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Zaquin, Tal
Di Bisceglie, Anna Paola
Pinkas, Iddo
Falini, Giuseppe
Mass, Tali
Different skeletal protein toolkits achieve similar structure and performance in the tropical coral Stylophora pistillata and the temperate Oculina patagonica
title Different skeletal protein toolkits achieve similar structure and performance in the tropical coral Stylophora pistillata and the temperate Oculina patagonica
title_full Different skeletal protein toolkits achieve similar structure and performance in the tropical coral Stylophora pistillata and the temperate Oculina patagonica
title_fullStr Different skeletal protein toolkits achieve similar structure and performance in the tropical coral Stylophora pistillata and the temperate Oculina patagonica
title_full_unstemmed Different skeletal protein toolkits achieve similar structure and performance in the tropical coral Stylophora pistillata and the temperate Oculina patagonica
title_short Different skeletal protein toolkits achieve similar structure and performance in the tropical coral Stylophora pistillata and the temperate Oculina patagonica
title_sort different skeletal protein toolkits achieve similar structure and performance in the tropical coral stylophora pistillata and the temperate oculina patagonica
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9532382/
https://www.ncbi.nlm.nih.gov/pubmed/36195656
http://dx.doi.org/10.1038/s41598-022-20744-0
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