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(Greenlip Abalone) Nacre and Prismatic Organic Shell Matrix Karlheinz Mann1* , Nicolas Cerveau2, Meike Gummich3, Monika Fritz3, Matthias Mann1 and Daniel J

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(Greenlip Abalone) Nacre and Prismatic Organic Shell Matrix Karlheinz Mann1* , Nicolas Cerveau2, Meike Gummich3, Monika Fritz3, Matthias Mann1 and Daniel J Mann et al. Proteome Science (2018) 16:11 https://doi.org/10.1186/s12953-018-0139-3 RESEARCH Open Access In-depth proteomic analyses of Haliotis laevigata (greenlip abalone) nacre and prismatic organic shell matrix Karlheinz Mann1* , Nicolas Cerveau2, Meike Gummich3, Monika Fritz3, Matthias Mann1 and Daniel J. Jackson2 Abstract Background: The shells of various Haliotis species have served as models of invertebrate biomineralization and physical shell properties for more than 20 years. A focus of this research has been the nacreous inner layer of the shell with its conspicuous arrangement of aragonite platelets, resembling in cross-section a brick-and-mortar wall. In comparison, the outer, less stable, calcitic prismatic layer has received much less attention. One of the first molluscan shell proteins to be characterized at the molecular level was Lustrin A, a component of the nacreous organic matrix of Haliotis rufescens. This was soon followed by the C-type lectin perlucin and the growth factor-binding perlustrin, both isolated from H. laevigata nacre, and the crystal growth-modulating AP7 and AP24, isolated from H. rufescens nacre. Mass spectrometry-based proteomics was subsequently applied to to Haliotis biomineralization research with the analysis of the H. asinina shell matrix and yielded 14 different shell-associated proteins. That study was the most comprehensive for a Haliotis species to date. Methods: The shell proteomes of nacre and prismatic layer of the marine gastropod Haliotis laevigata were analyzed combining mass spectrometry-based proteomics and next generation sequencing. Results: We identified 297 proteins from the nacreous shell layer and 350 proteins from the prismatic shell layer from the green lip abalone H. laevigata. Considering the overlap between the two sets we identified a total of 448 proteins. Fifty-one nacre proteins and 43 prismatic layer proteins were defined as major proteins based on their abundance at more than 0.2% of the total. The remaining proteins occurred at low abundance and may not play any significant role in shell fabrication. The overlap of major proteins between the two shell layers was 17, amounting to a total of 77 major proteins. Conclusions: The H. laevigata shell proteome shares moderate sequence similarity at the protein level with other gastropod, bivalve and more distantly related invertebrate biomineralising proteomes. Features conserved in H. laevigata and other molluscan shell proteomes include short repetitive sequences of low complexity predicted to lack intrinsic three-dimensional structure, and domains such as tyrosinase, chitin-binding, and carbonic anhydrase. This catalogue of H. laevigata shell proteins represents the most comprehensive for a haliotid and should support future efforts to elucidate the molecular mechanisms of shell assembly. Keywords: Biomineralization, Mantle transcriptome, Shell organic matrix, Nacre, Prismatic layer, Proteome * Correspondence: [email protected] 1Abteilung Proteomics und Signaltransduktion, Max-Planck-Institut für Biochemie, Am Klopferspitz 18, D-82152 Martinsried, Germany Full list of author information is available at the end of the article © The Author(s). 2018 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Mann et al. Proteome Science (2018) 16:11 Page 2 of 25 Background Perlwapin was the only protein among these 21 that had Species of the gastropod genus Haliotis construct a shell been previously identified. The study on H. asinina [21] with two clearly distinguishable major layers, prismatic compared the proteomes of the entire shell and nacre and nacreous, both of which are a composite of mineral- alone. Five proteins were identified in the whole shell but ized CaCO3 and organic molecules [1, 2]. The outer, rela- not in nacre, indicating that they were restricted to the tively soft and chalky prismatic layer is comprised of prismatic layer and may induce the formation of prisms or prism-shaped crystals. The inner mother-of-pearl layer, or the inhibition of nacre. Similarly, differences in protein nacre, is characterized by thin intercalated plates and has composition were also found in more comprehensive attracted much more interest as a model in biomaterials studies of separate shell layers of the pearl oysters Pinc- and biomineralization research than the prismatic layer. tada margaritifera and P. maxima [23] and various Myti- This is due to its extraordinary toughness and fracture re- lus species [24, 25]. sistance conferred by the arrangement of individual ara- Next generation sequencing (NGS) techniques have gonite crystals which are connected by mineral bridges developed rapidly and allow for the rapid sequencing of and enclosed by a thin layer of organic matrix [3–6]. entire genomes and transcriptomes that can be used to In both layers the crystals are enveloped and pervaded study not only the expression of biomineralization-related by an organic matrix that constitutes approximately 2% of genes, but also as sequence databases for more compre- the total bio-composite weight, and which is composed hensive proteomic studies. In the present report we have predominantly of protein and polysaccharide. The mineral conducted an in-depth proteomic analysis of the separated and organic precursors of the shell are secreted by the prismatic and nacreous layer organic matrices of H. laevi- mantle epithelium that lines the extrapallial space between gata coupled with transcriptomic sequencing of Haliotis mantle tissue and the shell [7]. The secreted organic mantle tissue. The resulting shell-associated proteome matrix is thought to assemble extracellularly and to pro- included almost all previously identified Haliotis proteins vide a mold that templates and guides the growth of the as well as many new proteins that were annotated with mineral [4]. In fact isolated H. rufescens organic shell respect to abundance, similarity to other proteins, pre- matrix was shown to control nucleation, crystal orienta- dicted domain structure, predicted secretion signal pep- tion, the nature of the calcium carbonate polymorph de- tide and transmembrane segments, isoelectric point, posited [8–11], and to act as an adhesive between the amino acid composition, and predicted intrinsic disorder. aragonitic plates [12]. We have also compared these proteins with similarly The search for individual proteins responsible for these derived datasets from a range of other molluscs and more effects by molecular biological and biochemical methods distantly related invertebrates in order to determine what lead to the discovery in H. rufescens nacre of lustrin A, a broad level of sequence similarity exists between these large multi-domain protein [13] that is localised immuno- biomineralising proteomes. histochemically to the extra-crystalline matrix between nacre plates [12]. Other Haliotis proteins isolated and Methods characterized include the mineral-binding C-type lectin Preparation of matrix and peptides perlucin [14, 15], the IGF-binding protein perlustrin [16], Haliotis laevigata shells of lengths of 15-18 cm and the mineral-binding proteins AP7 and AP24 [17], the weights of 150-200 g were treated with a final concen- crystal morphology-modifying AP8 proteins [18], the crys- tration of 4% sodium hypochlorite solution (Carl Roth, tal growth-inhibitor perlwapin [19], and perlinhibins, Karlsruhe, Germany) for 2 h without (method A) or with low-abundance Cys-, His- and Arg-rich mini-proteins that (method B) a 5 min ultrasound treatment at the start of inhibit calcium carbonate crystallization [20]. More re- each hour. Shells were then washed extensively with cently increased application of mass spectrometry-based deionized water and dried. Alternatively, the nacreous proteomic techniques to biomineral matrices has enabled layer of a shell not washed with hypochlorite before was the identification of comparatively large numbers of pro- sand-blasted from each side to remove possible contami- teins in a short time without the need to resort to compli- nants (method C). Nacre matrix was prepared as cated protein separation protocols. However, for these described previously [26]. For prismatic shell layer prepar- proteomic methods one still requires sequence databases ation the surface of shells was cleaned mechanically to re- as comprehensive as possible to obtain meaningful results. move mineralized worm tubes and other material not Examples of the application of such proteomic methods to belonging to the shell. Shells were then washed with hypo- haliotids with relatively limited EST databases created by chlorite as before (methods A and B) and the prismatic Sanger sequencing include analyses of the shell organic shell layer was filed off and collected for demineralization. matrix in H. asinina [21]andH. tuberculata [22]. Calcite powder and nacre pieces were dissolved in 12% Altogether 21 proteins were identified by searching mass acetic acid and the suspension was dialyzed and stored in spectra against translated EST
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