The skeletal proteome of the coral Acropora millepora: the evolution of calcification by co-option and domain shuffling.

14 pages International audience In corals, biocalcification is a major function that may be drastically affected by ocean acidification (OA). Scleractinian corals grow by building up aragonitic exoskeletons that provide support and protection for soft tissues. Although this process has been extensiv...

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Published in:Molecular Biology and Evolution
Main Authors: Ramos-Silva, Paula, Kaandorp, Jaap, Huisman, Lotte, Marie, Benjamin, Zanella-Cléon, Isabelle, Guichard, Nathalie, Miller, David J., Marin, Frédéric
Other Authors: Biogéosciences UMR 6282 (BGS), Université de Bourgogne (UB)-Centre National de la Recherche Scientifique (CNRS), Section Computational Science, University of Amsterdam Amsterdam = Universiteit van Amsterdam (UvA), ARC Centre of Excellence for Coral Reef Studies (CoralCoE), James Cook University (JCU), Molécules de Communication et Adaptation des Micro-Organismes (MCAM), Muséum national d'Histoire naturelle (MNHN)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Centre National de la Recherche Scientifique (CNRS), BioSciences Lyon-Gerland (BLG), École normale supérieure de Lyon (ENS de Lyon)-Institut National de la Recherche Agronomique (INRA)-Université Claude Bernard Lyon 1 (UCBL), Université de Lyon-Université de Lyon-Hospices Civils de Lyon (HCL)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Centre National de la Recherche Scientifique (CNRS), Work supported by the EU FP7 Marie Curie Initial Training Network BIOMINTEC (PITNGA-2008-215507, www.biomintec.de, coordinator H.C. Schröder), by the EU FP7 Knowledge Based Bio-Economy project BioPreDyn grant 289434 (www.biopredyn.eu), and by the COST project TD0903 ("Biomineralix", www.biomineralix.eu, 2009-2013)
Format: Article in Journal/Newspaper
Language:English
Published: HAL CCSD 2013
Subjects:
Online Access:https://hal.science/hal-00853820
https://doi.org/10.1093/molbev/mst109
id ftccsdartic:oai:HAL:hal-00853820v1
record_format openpolar
institution Open Polar
collection Archive ouverte HAL (Hyper Article en Ligne, CCSD - Centre pour la Communication Scientifique Directe)
op_collection_id ftccsdartic
language English
topic biomineralization
calcium carbonate skeleton
scleractinian
proteomics
evolution
[SDV.IB.BIO]Life Sciences [q-bio]/Bioengineering/Biomaterials
[SDV.BBM.GTP]Life Sciences [q-bio]/Biochemistry
Molecular Biology/Genomics [q-bio.GN]
spellingShingle biomineralization
calcium carbonate skeleton
scleractinian
proteomics
evolution
[SDV.IB.BIO]Life Sciences [q-bio]/Bioengineering/Biomaterials
[SDV.BBM.GTP]Life Sciences [q-bio]/Biochemistry
Molecular Biology/Genomics [q-bio.GN]
Ramos-Silva, Paula
Kaandorp, Jaap
Huisman, Lotte
Marie, Benjamin
Zanella-Cléon, Isabelle
Guichard, Nathalie
Miller, David J.
Marin, Frédéric
The skeletal proteome of the coral Acropora millepora: the evolution of calcification by co-option and domain shuffling.
topic_facet biomineralization
calcium carbonate skeleton
scleractinian
proteomics
evolution
[SDV.IB.BIO]Life Sciences [q-bio]/Bioengineering/Biomaterials
[SDV.BBM.GTP]Life Sciences [q-bio]/Biochemistry
Molecular Biology/Genomics [q-bio.GN]
description 14 pages International audience In corals, biocalcification is a major function that may be drastically affected by ocean acidification (OA). Scleractinian corals grow by building up aragonitic exoskeletons that provide support and protection for soft tissues. Although this process has been extensively studied, the molecular basis of biocalcification is poorly understood. Notably lacking is a comprehensive catalog of the skeleton-occluded proteins-the skeletal organic matrix proteins (SOMPs) that are thought to regulate the mineral deposition. Using a combination of proteomics and transcriptomics, we report the first survey of such proteins in the staghorn coral Acropora millepora. The organic matrix (OM) extracted from the coral skeleton was analyzed by mass spectrometry and bioinformatics, enabling the identification of 36 SOMPs. These results provide novel insights into the molecular basis of coral calcification and the macroevolution of metazoan calcifying systems, whereas establishing a platform for studying the impact of OA at molecular level. Besides secreted proteins, extracellular regions of transmembrane proteins are also present, suggesting a close control of aragonite deposition by the calicoblastic epithelium. In addition to the expected SOMPs (Asp/Glu-rich, galaxins), the skeletal repertoire included several proteins containing known extracellular matrix domains. From an evolutionary perspective, the number of coral-specific proteins is low, many SOMPs having counterparts in the noncalcifying cnidarians. Extending the comparison with the skeletal OM proteomes of other metazoans allowed the identification of a pool of functional domains shared between phyla. These data suggest that co-option and domain shuffling may be general mechanisms by which the trait of calcification has evolved.
author2 Biogéosciences UMR 6282 (BGS)
Université de Bourgogne (UB)-Centre National de la Recherche Scientifique (CNRS)
Section Computational Science
University of Amsterdam Amsterdam = Universiteit van Amsterdam (UvA)
ARC Centre of Excellence for Coral Reef Studies (CoralCoE)
James Cook University (JCU)
Molécules de Communication et Adaptation des Micro-Organismes (MCAM)
Muséum national d'Histoire naturelle (MNHN)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Centre National de la Recherche Scientifique (CNRS)
BioSciences Lyon-Gerland (BLG)
École normale supérieure de Lyon (ENS de Lyon)-Institut National de la Recherche Agronomique (INRA)-Université Claude Bernard Lyon 1 (UCBL)
Université de Lyon-Université de Lyon-Hospices Civils de Lyon (HCL)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Centre National de la Recherche Scientifique (CNRS)
Work supported by the EU FP7 Marie Curie Initial Training Network BIOMINTEC (PITNGA-2008-215507, www.biomintec.de, coordinator H.C. Schröder), by the EU FP7 Knowledge Based Bio-Economy project BioPreDyn grant 289434 (www.biopredyn.eu), and by the COST project TD0903 ("Biomineralix", www.biomineralix.eu, 2009-2013)
format Article in Journal/Newspaper
author Ramos-Silva, Paula
Kaandorp, Jaap
Huisman, Lotte
Marie, Benjamin
Zanella-Cléon, Isabelle
Guichard, Nathalie
Miller, David J.
Marin, Frédéric
author_facet Ramos-Silva, Paula
Kaandorp, Jaap
Huisman, Lotte
Marie, Benjamin
Zanella-Cléon, Isabelle
Guichard, Nathalie
Miller, David J.
Marin, Frédéric
author_sort Ramos-Silva, Paula
title The skeletal proteome of the coral Acropora millepora: the evolution of calcification by co-option and domain shuffling.
title_short The skeletal proteome of the coral Acropora millepora: the evolution of calcification by co-option and domain shuffling.
title_full The skeletal proteome of the coral Acropora millepora: the evolution of calcification by co-option and domain shuffling.
title_fullStr The skeletal proteome of the coral Acropora millepora: the evolution of calcification by co-option and domain shuffling.
title_full_unstemmed The skeletal proteome of the coral Acropora millepora: the evolution of calcification by co-option and domain shuffling.
title_sort skeletal proteome of the coral acropora millepora: the evolution of calcification by co-option and domain shuffling.
publisher HAL CCSD
publishDate 2013
url https://hal.science/hal-00853820
https://doi.org/10.1093/molbev/mst109
genre Ocean acidification
genre_facet Ocean acidification
op_source ISSN: 0737-4038
EISSN: 1537-1719
Molecular Biology and Evolution
https://hal.science/hal-00853820
Molecular Biology and Evolution, 2013, 30 (9), pp.2099-2112. ⟨10.1093/molbev/mst109⟩
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doi:10.1093/molbev/mst109
PUBMED: 23765379
PUBMEDCENTRAL: PMC3748352
op_doi https://doi.org/10.1093/molbev/mst109
container_title Molecular Biology and Evolution
container_volume 30
container_issue 9
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spelling ftccsdartic:oai:HAL:hal-00853820v1 2024-02-11T10:07:35+01:00 The skeletal proteome of the coral Acropora millepora: the evolution of calcification by co-option and domain shuffling. Ramos-Silva, Paula Kaandorp, Jaap Huisman, Lotte Marie, Benjamin Zanella-Cléon, Isabelle Guichard, Nathalie Miller, David J. Marin, Frédéric Biogéosciences UMR 6282 (BGS) Université de Bourgogne (UB)-Centre National de la Recherche Scientifique (CNRS) Section Computational Science University of Amsterdam Amsterdam = Universiteit van Amsterdam (UvA) ARC Centre of Excellence for Coral Reef Studies (CoralCoE) James Cook University (JCU) Molécules de Communication et Adaptation des Micro-Organismes (MCAM) Muséum national d'Histoire naturelle (MNHN)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Centre National de la Recherche Scientifique (CNRS) BioSciences Lyon-Gerland (BLG) École normale supérieure de Lyon (ENS de Lyon)-Institut National de la Recherche Agronomique (INRA)-Université Claude Bernard Lyon 1 (UCBL) Université de Lyon-Université de Lyon-Hospices Civils de Lyon (HCL)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Centre National de la Recherche Scientifique (CNRS) Work supported by the EU FP7 Marie Curie Initial Training Network BIOMINTEC (PITNGA-2008-215507, www.biomintec.de, coordinator H.C. Schröder), by the EU FP7 Knowledge Based Bio-Economy project BioPreDyn grant 289434 (www.biopredyn.eu), and by the COST project TD0903 ("Biomineralix", www.biomineralix.eu, 2009-2013) 2013-09 https://hal.science/hal-00853820 https://doi.org/10.1093/molbev/mst109 en eng HAL CCSD Oxford University Press (OUP) info:eu-repo/semantics/altIdentifier/doi/10.1093/molbev/mst109 info:eu-repo/semantics/altIdentifier/pmid/23765379 hal-00853820 https://hal.science/hal-00853820 doi:10.1093/molbev/mst109 PUBMED: 23765379 PUBMEDCENTRAL: PMC3748352 ISSN: 0737-4038 EISSN: 1537-1719 Molecular Biology and Evolution https://hal.science/hal-00853820 Molecular Biology and Evolution, 2013, 30 (9), pp.2099-2112. ⟨10.1093/molbev/mst109⟩ biomineralization calcium carbonate skeleton scleractinian proteomics evolution [SDV.IB.BIO]Life Sciences [q-bio]/Bioengineering/Biomaterials [SDV.BBM.GTP]Life Sciences [q-bio]/Biochemistry Molecular Biology/Genomics [q-bio.GN] info:eu-repo/semantics/article Journal articles 2013 ftccsdartic https://doi.org/10.1093/molbev/mst109 2024-01-27T23:29:20Z 14 pages International audience In corals, biocalcification is a major function that may be drastically affected by ocean acidification (OA). Scleractinian corals grow by building up aragonitic exoskeletons that provide support and protection for soft tissues. Although this process has been extensively studied, the molecular basis of biocalcification is poorly understood. Notably lacking is a comprehensive catalog of the skeleton-occluded proteins-the skeletal organic matrix proteins (SOMPs) that are thought to regulate the mineral deposition. Using a combination of proteomics and transcriptomics, we report the first survey of such proteins in the staghorn coral Acropora millepora. The organic matrix (OM) extracted from the coral skeleton was analyzed by mass spectrometry and bioinformatics, enabling the identification of 36 SOMPs. These results provide novel insights into the molecular basis of coral calcification and the macroevolution of metazoan calcifying systems, whereas establishing a platform for studying the impact of OA at molecular level. Besides secreted proteins, extracellular regions of transmembrane proteins are also present, suggesting a close control of aragonite deposition by the calicoblastic epithelium. In addition to the expected SOMPs (Asp/Glu-rich, galaxins), the skeletal repertoire included several proteins containing known extracellular matrix domains. From an evolutionary perspective, the number of coral-specific proteins is low, many SOMPs having counterparts in the noncalcifying cnidarians. Extending the comparison with the skeletal OM proteomes of other metazoans allowed the identification of a pool of functional domains shared between phyla. These data suggest that co-option and domain shuffling may be general mechanisms by which the trait of calcification has evolved. Article in Journal/Newspaper Ocean acidification Archive ouverte HAL (Hyper Article en Ligne, CCSD - Centre pour la Communication Scientifique Directe) Molecular Biology and Evolution 30 9 2099 2112