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Correlative chemical and elemental nano-imaging of morphology and disorder at the nacre-prismatic region interface in Pinctada margaritifera
Understanding biomineralization relies on imaging chemically heterogeneous organic–inorganic interfaces across a hierarchy of spatial scales. Further, organic minority phases are often responsible for emergent inorganic structures from the atomic arrangement of different polymorphs, to nano- and mic...
Autores principales: | , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
Nature Publishing Group UK
2023
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10692121/ https://www.ncbi.nlm.nih.gov/pubmed/38040799 http://dx.doi.org/10.1038/s41598-023-47446-5 |
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author | O’Callahan, Brian T. Larsen, Amy Leichty, Sarah Cliff, John Gagnon, Alex C. Raschke, Markus B. |
author_facet | O’Callahan, Brian T. Larsen, Amy Leichty, Sarah Cliff, John Gagnon, Alex C. Raschke, Markus B. |
author_sort | O’Callahan, Brian T. |
collection | PubMed |
description | Understanding biomineralization relies on imaging chemically heterogeneous organic–inorganic interfaces across a hierarchy of spatial scales. Further, organic minority phases are often responsible for emergent inorganic structures from the atomic arrangement of different polymorphs, to nano- and micrometer crystal dimensions, up to meter size mollusk shells. The desired simultaneous chemical and elemental imaging to identify sparse organic moieties across a large field-of-view with nanometer spatial resolution has not yet been achieved. Here, we combine nanoscale secondary ion mass spectroscopy (NanoSIMS) with spectroscopic IR s-SNOM imaging for simultaneous chemical, molecular, and elemental nanoimaging. At the example of Pinctada margaritifera mollusk shells we identify and resolve ~ 50 nm interlamellar protein sheets periodically arranged in regular ~ 600 nm intervals. The striations typically appear ~ 15 µm from the nacre-prism boundary at the interface between disordered neonacre to mature nacre. Using the polymorph distinctive IR-vibrational carbonate resonance, the nacre and prismatic regions are consistently identified as aragonite ([Formula: see text] cm(−1)) and calcite ([Formula: see text] cm(−1)), respectively. We observe previously unreported morphological features including aragonite subdomains encapsulated in extensions of the prism-covering organic membrane and regions of irregular nacre tablet formation coincident with dispersed organics. We also identify a ~ 200 nm region in the incipient nacre region with less well-defined crystal structure and integrated organics. These results show with the identification of the interlamellar protein layer how correlative nano-IR chemical and NanoSIMS elemental imaging can help distinguish different models proposed for shell growth in particular, and how organic function may relate to inorganic structure in other biomineralized systems in general. |
format | Online Article Text |
id | pubmed-10692121 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2023 |
publisher | Nature Publishing Group UK |
record_format | MEDLINE/PubMed |
spelling | pubmed-106921212023-12-03 Correlative chemical and elemental nano-imaging of morphology and disorder at the nacre-prismatic region interface in Pinctada margaritifera O’Callahan, Brian T. Larsen, Amy Leichty, Sarah Cliff, John Gagnon, Alex C. Raschke, Markus B. Sci Rep Article Understanding biomineralization relies on imaging chemically heterogeneous organic–inorganic interfaces across a hierarchy of spatial scales. Further, organic minority phases are often responsible for emergent inorganic structures from the atomic arrangement of different polymorphs, to nano- and micrometer crystal dimensions, up to meter size mollusk shells. The desired simultaneous chemical and elemental imaging to identify sparse organic moieties across a large field-of-view with nanometer spatial resolution has not yet been achieved. Here, we combine nanoscale secondary ion mass spectroscopy (NanoSIMS) with spectroscopic IR s-SNOM imaging for simultaneous chemical, molecular, and elemental nanoimaging. At the example of Pinctada margaritifera mollusk shells we identify and resolve ~ 50 nm interlamellar protein sheets periodically arranged in regular ~ 600 nm intervals. The striations typically appear ~ 15 µm from the nacre-prism boundary at the interface between disordered neonacre to mature nacre. Using the polymorph distinctive IR-vibrational carbonate resonance, the nacre and prismatic regions are consistently identified as aragonite ([Formula: see text] cm(−1)) and calcite ([Formula: see text] cm(−1)), respectively. We observe previously unreported morphological features including aragonite subdomains encapsulated in extensions of the prism-covering organic membrane and regions of irregular nacre tablet formation coincident with dispersed organics. We also identify a ~ 200 nm region in the incipient nacre region with less well-defined crystal structure and integrated organics. These results show with the identification of the interlamellar protein layer how correlative nano-IR chemical and NanoSIMS elemental imaging can help distinguish different models proposed for shell growth in particular, and how organic function may relate to inorganic structure in other biomineralized systems in general. Nature Publishing Group UK 2023-12-01 /pmc/articles/PMC10692121/ /pubmed/38040799 http://dx.doi.org/10.1038/s41598-023-47446-5 Text en © This is a U.S. Government work and not under copyright protection in the US; foreign copyright protection may apply 2023 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 O’Callahan, Brian T. Larsen, Amy Leichty, Sarah Cliff, John Gagnon, Alex C. Raschke, Markus B. Correlative chemical and elemental nano-imaging of morphology and disorder at the nacre-prismatic region interface in Pinctada margaritifera |
title | Correlative chemical and elemental nano-imaging of morphology and disorder at the nacre-prismatic region interface in Pinctada margaritifera |
title_full | Correlative chemical and elemental nano-imaging of morphology and disorder at the nacre-prismatic region interface in Pinctada margaritifera |
title_fullStr | Correlative chemical and elemental nano-imaging of morphology and disorder at the nacre-prismatic region interface in Pinctada margaritifera |
title_full_unstemmed | Correlative chemical and elemental nano-imaging of morphology and disorder at the nacre-prismatic region interface in Pinctada margaritifera |
title_short | Correlative chemical and elemental nano-imaging of morphology and disorder at the nacre-prismatic region interface in Pinctada margaritifera |
title_sort | correlative chemical and elemental nano-imaging of morphology and disorder at the nacre-prismatic region interface in pinctada margaritifera |
topic | Article |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10692121/ https://www.ncbi.nlm.nih.gov/pubmed/38040799 http://dx.doi.org/10.1038/s41598-023-47446-5 |
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