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Biomineralization of Schlumbergerella floresiana, a significant carbonate-producing benthic foraminifer

Authors

  • A. Sabbatini,

    Corresponding author
    1. Department of Life and Environmental Sciences (Di.S.V.A.), Polytechnic University of Marche, Ancona, Italy
    2. Centre de Recherche sur la Paléobiodiversité et les Paléoenvironnements, UMR 7207 CNRS MNHN UPMC, Muséum National d'Histoire Naturelle, Paris Cedex 05, France
    • Corresponding author: A. Sabbatini. Tel.: 0039 0712204329; fax: 0039 0712204650; e-mail: a.sabbatini@univpm.it

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  • L. Bédouet,

    1. Biologie des Organismes et Ecosystèmes Aquatiques, UMR CNRS 7208/IRD 207, Muséum National d'Histoire Naturelle, Paris Cedex 05, France
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  • A. Marie,

    1. Département Régulation Développement et Diversité Moléculaire, UMR CNRS 7245, Plateforme de Spectrométrie de masse et de Protéomique, Muséum National d'Histoire Naturelle, Paris Cedex 05, France
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  • A. Bartolini,

    1. Centre de Recherche sur la Paléobiodiversité et les Paléoenvironnements, UMR 7207 CNRS MNHN UPMC, Muséum National d'Histoire Naturelle, Paris Cedex 05, France
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  • L. Landemarre,

    1. GLYcoDiag, UFR Sciences, Orléans Cedex 2, France
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  • M. X. Weber,

    1. Department of Biology, Pennsylvania State University, 208 Mueller Lab, University Park, PA 16802, USA
    2. Unidad Académica de Sistemas Arrecifales, Instituto de Ciencias del Mar y Limnologia, Universidad Nacional Autónoma de México, Puerto Morelos, Q. Roo, México
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  • I. Gusti Ngurah Kade Mahardika,

    1. The Animal Biomedical and Molecular Biology Laboratory, Udayana University, Bali, Indonesia
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  • S. Berland,

    1. Biologie des Organismes et Ecosystèmes Aquatiques, UMR CNRS 7208/IRD 207, Muséum National d'Histoire Naturelle, Paris Cedex 05, France
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  • F. Zito,

    1. Institut de Biologie Physico-Chimique, CNRS/Université Paris-7 UMR 7099, Paris, France
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  • M.-T. Vénec-Peyré

    1. Centre de Recherche sur la Paléobiodiversité et les Paléoenvironnements, UMR 7207 CNRS MNHN UPMC, Muséum National d'Histoire Naturelle, Paris Cedex 05, France
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Abstract

Most foraminifera that produce a shell are efficient biomineralizers. We analyzed the calcitic shell of the large tropical benthic foraminifer Schlumbergerella floresiana. We found a suite of macromolecules containing many charged and polar amino acids and glycine that are also abundant in biomineralization proteins of other phyla. As neither genomic nor transcriptomic data are available for foraminiferal biomineralization yet, de novo-generated sequences, obtained from organic matrices submitted to ms blast database search, led to the characterization of 156 peptides. Very few homologous proteins were matched in the proteomic database, implying that the peptides are derived from unknown proteins present in the foraminiferal organic matrices. The amino acid distribution of these peptides was queried against the uniprot database and the mollusk uniprot database for comparison. The mollusks compose a well-studied phylum that yield a large variety of biomineralization proteins. These results showed that proteins extracted from S. floresiana shells contained sequences enriched with glycine, alanine, and proline, making a set of residues that provided a signature unique to foraminifera. Three of the de novo peptides exhibited sequence similarities to peptides found in proteins such as pre-collagen-P and a group of P-type ATPases including a calcium-transporting ATPase. Surprisingly, the peptide that was most similar to the collagen-like protein was a glycine-rich peptide reported from the test and spine proteome of sea urchin. The molecules, identified by matrix-assisted laser desorption ionization-time of flight mass spectrometry analyses, included acid-soluble N-glycoproteins with its sugar moieties represented by high-mannose-type glycans and carbohydrates. Describing the nature of the proteins, and associated molecules in the skeletal structure of living foraminifera, can elucidate the biomineralization mechanisms of these major carbonate producers in marine ecosystems. As fossil foraminifera provide important paleoenvironmental and paleoclimatic information, a better understanding of biomineralization in these organisms will have far-reaching impacts.

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