Evolution and diversity of biomineralized columnar architecture in early Cambrian phosphatic-shelled brachiopods

Biologically-controlled mineralization producing organic-inorganic composites (hard skeletons) by metazoan biomineralizers has been an evolutionary innovation since the earliest Cambrian. Among them, linguliform brachiopods are one of the key invertebrates that secrete calcium phosphate minerals to...

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Main Authors: Zhiliang Zhang, Zhifei Zhang, Lars Holmer, Timothy P Topper, Bing Pan, Guoxiang Li
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2024-04-01
Series:eLife
Subjects:
Online Access:https://elifesciences.org/articles/88855
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author Zhiliang Zhang
Zhifei Zhang
Lars Holmer
Timothy P Topper
Bing Pan
Guoxiang Li
author_facet Zhiliang Zhang
Zhifei Zhang
Lars Holmer
Timothy P Topper
Bing Pan
Guoxiang Li
author_sort Zhiliang Zhang
collection DOAJ
description Biologically-controlled mineralization producing organic-inorganic composites (hard skeletons) by metazoan biomineralizers has been an evolutionary innovation since the earliest Cambrian. Among them, linguliform brachiopods are one of the key invertebrates that secrete calcium phosphate minerals to build their shells. One of the most distinct shell structures is the organo-phosphatic cylindrical column exclusive to phosphatic-shelled brachiopods, including both crown and stem groups. However, the complexity, diversity, and biomineralization processes of these microscopic columns are far from clear in brachiopod ancestors. Here, exquisitely well-preserved columnar shell ultrastructures are reported for the first time in the earliest eoobolids Latusobolus xiaoyangbaensis gen. et sp. nov. and Eoobolus acutulus sp. nov. from the Cambrian Series 2 Shuijingtuo Formation of South China. The hierarchical shell architectures, epithelial cell moulds, and the shape and size of cylindrical columns are scrutinised in these new species. Their calcium phosphate-based biomineralized shells are mainly composed of stacked sandwich columnar units. The secretion and construction of the stacked sandwich model of columnar architecture, which played a significant role in the evolution of linguliforms, is highly biologically controlled and organic-matrix mediated. Furthermore, a continuous transformation of anatomic features resulting from the growth of diverse columnar shells is revealed between Eoobolidae, Lingulellotretidae, and Acrotretida, shedding new light on the evolutionary growth and adaptive innovation of biomineralized columnar architecture among early phosphatic-shelled brachiopods during the Cambrian explosion.
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spelling doaj.art-79fd3d2520664b4185521735d061c2382024-04-10T14:21:18ZengeLife Sciences Publications LtdeLife2050-084X2024-04-011210.7554/eLife.88855Evolution and diversity of biomineralized columnar architecture in early Cambrian phosphatic-shelled brachiopodsZhiliang Zhang0https://orcid.org/0000-0003-2296-5973Zhifei Zhang1https://orcid.org/0000-0003-0325-5116Lars Holmer2Timothy P Topper3https://orcid.org/0000-0001-6720-7418Bing Pan4https://orcid.org/0000-0002-7457-2517Guoxiang Li5State Key Laboratory of Palaeobiology and Stratigraphy, Nanjing Institute of Geology and Palaeontology, Chinese Academy of Sciences, Nanjing, China; School of Natural Sciences, Macquarie University, Macquarie Park, AustraliaState Key Laboratory of Continental Dynamics, Shaanxi Key Laboratory of Early Life & Environments, Department of Geology, Northwest University, Xi'an, ChinaInstitute of Earth Sciences, Palaeobiology, Uppsala University, Uppsala, SwedenState Key Laboratory of Continental Dynamics, Shaanxi Key Laboratory of Early Life & Environments, Department of Geology, Northwest University, Xi'an, China; Department of Palaeobiology, Swedish Museum of Natural History Stockholm, Stockholm, SwedenState Key Laboratory of Palaeobiology and Stratigraphy, Nanjing Institute of Geology and Palaeontology, Chinese Academy of Sciences, Nanjing, ChinaState Key Laboratory of Palaeobiology and Stratigraphy, Nanjing Institute of Geology and Palaeontology, Chinese Academy of Sciences, Nanjing, ChinaBiologically-controlled mineralization producing organic-inorganic composites (hard skeletons) by metazoan biomineralizers has been an evolutionary innovation since the earliest Cambrian. Among them, linguliform brachiopods are one of the key invertebrates that secrete calcium phosphate minerals to build their shells. One of the most distinct shell structures is the organo-phosphatic cylindrical column exclusive to phosphatic-shelled brachiopods, including both crown and stem groups. However, the complexity, diversity, and biomineralization processes of these microscopic columns are far from clear in brachiopod ancestors. Here, exquisitely well-preserved columnar shell ultrastructures are reported for the first time in the earliest eoobolids Latusobolus xiaoyangbaensis gen. et sp. nov. and Eoobolus acutulus sp. nov. from the Cambrian Series 2 Shuijingtuo Formation of South China. The hierarchical shell architectures, epithelial cell moulds, and the shape and size of cylindrical columns are scrutinised in these new species. Their calcium phosphate-based biomineralized shells are mainly composed of stacked sandwich columnar units. The secretion and construction of the stacked sandwich model of columnar architecture, which played a significant role in the evolution of linguliforms, is highly biologically controlled and organic-matrix mediated. Furthermore, a continuous transformation of anatomic features resulting from the growth of diverse columnar shells is revealed between Eoobolidae, Lingulellotretidae, and Acrotretida, shedding new light on the evolutionary growth and adaptive innovation of biomineralized columnar architecture among early phosphatic-shelled brachiopods during the Cambrian explosion.https://elifesciences.org/articles/88855biomineralizationphosphatic-shelledcolumnar architecturecambrian explosionbrachiopodsbiologically controlled
spellingShingle Zhiliang Zhang
Zhifei Zhang
Lars Holmer
Timothy P Topper
Bing Pan
Guoxiang Li
Evolution and diversity of biomineralized columnar architecture in early Cambrian phosphatic-shelled brachiopods
eLife
biomineralization
phosphatic-shelled
columnar architecture
cambrian explosion
brachiopods
biologically controlled
title Evolution and diversity of biomineralized columnar architecture in early Cambrian phosphatic-shelled brachiopods
title_full Evolution and diversity of biomineralized columnar architecture in early Cambrian phosphatic-shelled brachiopods
title_fullStr Evolution and diversity of biomineralized columnar architecture in early Cambrian phosphatic-shelled brachiopods
title_full_unstemmed Evolution and diversity of biomineralized columnar architecture in early Cambrian phosphatic-shelled brachiopods
title_short Evolution and diversity of biomineralized columnar architecture in early Cambrian phosphatic-shelled brachiopods
title_sort evolution and diversity of biomineralized columnar architecture in early cambrian phosphatic shelled brachiopods
topic biomineralization
phosphatic-shelled
columnar architecture
cambrian explosion
brachiopods
biologically controlled
url https://elifesciences.org/articles/88855
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