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      'Palaeoshellomics’ reveals the use of freshwater mother-of-pearl in prehistory

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          Abstract

          The extensive use of mollusc shell as a versatile raw material is testament to its importance in prehistoric times. The consistent choice of certain species for different purposes, including the making of ornaments, is a direct representation of how humans viewed and exploited their environment. The necessary taxonomic information, however, is often impossible to obtain from objects that are small, heavily worked or degraded. Here we propose a novel biogeochemical approach to track the biological origin of prehistoric mollusc shell. We conducted an in-depth study of archaeological ornaments using microstructural, geochemical and biomolecular analyses, including ‘palaeoshellomics’, the first application of palaeoproteomics to mollusc shells (and indeed to any invertebrate calcified tissue). We reveal the consistent use of locally-sourced freshwater mother-of-pearl for the standardized manufacture of ‘double-buttons’. This craft is found throughout Europe between 4200–3800 BCE, highlighting the ornament-makers’ profound knowledge of the biogeosphere and the existence of cross-cultural traditions.

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          Just like people do today, prehistoric humans liked to adorn themselves with beautiful objects. Shells, from creatures like clams and snails, were used to decorate clothing or worn as jewelry at least as far back as 100,000 years ago. Later people used shells as the raw materials to make beads or bracelets. Learning where the shells came from may help scientists understand why prehistoric people chose certain shells and not others. It may also offer clues about how they used natural resources and the cultural significance of these objects. But identifying the shells is difficult because they lose many of their original distinctive features when worked into ornaments.

          New tools that use DNA or proteins to identify the raw materials used to craft ancient artifacts have emerged that may help. So far, scientists have mostly used these genomic and proteomic tools to identify the source of materials made from animal hide, ivory or bone – where collagen is the most abundant protein molecule. Yet it is more challenging to extract and characterize proteins or genetic material from mollusc shells. This is partly because the amount of proteins in shells is at least 300 times lower than in bone, and also because the makeup of proteins in shells is not as well-known as in collagen.

          Sakalauskaite et al. have now overcome these issues by combining the analytical tools used to study the proteins and mineral content of modern shells with those of ancient protein research. They then used this approach, which they named palaeoshellomics, to extract proteins from seven “double-buttons” – pearl-like ornaments crafted by prehistoric people in Europe. The double-buttons were made between 4200 and 3800 BC and found at archeological sites in Denmark, Germany and Romania. Comparing the extracted proteins to those from various mollusc shells showed that the double-buttons were made from freshwater mussels belonging to a group known as the Unionoida.

          The discovery helps settle a decade-long debate in archeology about the origin of the shells used to make double-buttons in prehistoric Europe. Ancient people often crafted ornaments from marine shells, because they were exotic and considered more prestigious. But the results on the double-buttons suggest instead that mother-of-pearl from fresh water shells was valued and used by groups throughout Europe, even those living in coastal areas. The palaeoshellomics technique used by Sakalauskaite et al. may now help identify the origins of shells from archeological and palaeontological sites.

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          The Proteomics Identifications (PRIDE) database and associated tools: status in 2013

          The PRoteomics IDEntifications (PRIDE, http://www.ebi.ac.uk/pride) database at the European Bioinformatics Institute is one of the most prominent data repositories of mass spectrometry (MS)-based proteomics data. Here, we summarize recent developments in the PRIDE database and related tools. First, we provide up-to-date statistics in data content, splitting the figures by groups of organisms and species, including peptide and protein identifications, and post-translational modifications. We then describe the tools that are part of the PRIDE submission pipeline, especially the recently developed PRIDE Converter 2 (new submission tool) and PRIDE Inspector (visualization and analysis tool). We also give an update about the integration of PRIDE with other MS proteomics resources in the context of the ProteomeXchange consortium. Finally, we briefly review the quality control efforts that are ongoing at present and outline our future plans.
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            PEAKS: powerful software for peptide de novo sequencing by tandem mass spectrometry.

            A number of different approaches have been described to identify proteins from tandem mass spectrometry (MS/MS) data. The most common approaches rely on the available databases to match experimental MS/MS data. These methods suffer from several drawbacks and cannot be used for the identification of proteins from unknown genomes. In this communication, we describe a new de novo sequencing software package, PEAKS, to extract amino acid sequence information without the use of databases. PEAKS uses a new model and a new algorithm to efficiently compute the best peptide sequences whose fragment ions can best interpret the peaks in the MS/MS spectrum. The output of the software gives amino acid sequences with confidence scores for the entire sequences, as well as an additional novel positional scoring scheme for portions of the sequences. The performance of PEAKS is compared with Lutefisk, a well-known de novo sequencing software, using quadrupole-time-of-flight (Q-TOF) data obtained for several tryptic peptides from standard proteins. Copyright 2003 John Wiley & Sons, Ltd.
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              The Global Decline of Nonmarine Mollusks

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                Author and article information

                Contributors
                Role: Senior Editor
                Role: Reviewing Editor
                Journal
                eLife
                Elife
                eLife
                eLife
                eLife Sciences Publications, Ltd
                2050-084X
                07 May 2019
                2019
                : 8
                : e45644
                Affiliations
                [1 ]deptDepartment of Life Sciences and Systems Biology University of Turin TurinItaly
                [2 ]deptUMR CNRS 6282 Biogéosciences University of Burgundy-Franche-Comté DijonFrance
                [3 ]Moesgaard Museum HøjbjergDenmark
                [4 ]deptDepartment of Asian and North African Studies University of Ca’ Foscari VeniceItaly
                [5 ]Independent researcher GenèveSwitzerland
                [6 ]deptDepartment of Archaeology University of York HeslingtonUnited Kingdom
                [7 ]deptDepartment of Molecular Biotechnology and Health Sciences University of Turin TurinItaly
                [8 ]Italian Malacological Society SorengoSwitzerland
                [9 ]Niedersächsisches Landesamt für Denkmalpflege HannoverGermany
                [10 ]deptSchool of Archaeological and Forensic Sciences University of Bradford BradfordUnited Kingdom
                [11 ]deptCentre for Experimental and Clinical Studies University of Turin TurinItaly
                [12 ]deptDepartment of Chemistry University of York HeslingtonUnited Kingdom
                [13 ]Institute of Molecular Chemistry, ICMUB UMR CNRS 6302, University of Burgundy-Franche-Comté DijonFrance
                [14 ]Landesamt für Denkmalpflege im Regierungspräsidium Stuttgart GaienhofenGermany
                [15 ]deptMiniaturization for Synthesis, Analysis & Proteomics USR CNRS 3290, University of Lille LilleFrance
                [16 ]deptDepartment of Mathematics University of York HeslingtonUnited Kingdom
                Max Planck Institute for Developmental Biology Germany
                Yale University United States
                Yale University United States
                Durham University United Kingdom
                Author notes
                [†]

                Institute of Chemistry & Biology of Membranes & Nano-objects, UMR CNRS 5248, Proteome Platform, University of Bordeaux, Bordeaux, France.

                Author information
                https://orcid.org/0000-0002-8029-8120
                http://orcid.org/0000-0003-0726-3025
                https://orcid.org/0000-0002-6226-9799
                http://orcid.org/0000-0002-1602-4416
                https://orcid.org/0000-0002-8398-4409
                Article
                45644
                10.7554/eLife.45644
                6542584
                31060688
                95e118a6-2036-48e4-aeab-6e9454e347bd
                © 2019, Sakalauskaite et al

                This article is distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use and redistribution provided that the original author and source are credited.

                History
                : 30 January 2019
                : 20 April 2019
                Funding
                Funded by: FundRef http://dx.doi.org/10.13039/501100003407, Ministry of Education, Universities and Research;
                Award ID: Young Researchers
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/501100000780, European Commission;
                Award ID: PERG-GA-2010-268429
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/501100000275, Leverhulme Trust;
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/501100004794, Centre National de la Recherche Scientifique;
                Award Recipient :
                Funded by: Campus France, Università Italo-Francese;
                Award ID: PHC Galilée programme
                Award Recipient :
                The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
                Categories
                Research Article
                Biochemistry and Chemical Biology
                Evolutionary Biology
                Custom metadata
                Ancient proteomes from tiny shell ornaments were successfully characterised for the first time, showing the unexpected use of mother-of-pearl from local riverine molluscs in both coastal and inland prehistoric sites.

                Life sciences
                mollusc shells,biomineralization,palaeoproteomics,tandem mass spectrometry,prehistory,ornaments,other

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