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Conservation of Three-Dimensional Structure of Lepidoptera and Trichoptera L-Fibroins for 290 Million Years

The divergence of sister orders Trichoptera (caddisflies) and Lepidoptera (moths and butterflies) from a silk-spinning ancestor occurred around 290 million years ago. Trichoptera larvae are mainly aquatic, and Lepidoptera larvae are almost entirely terrestrial—distinct habitats that required molecul...

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Autores principales: Stewart, Russell J., Frandsen, Paul B., Pauls, Steffen U., Heckenhauer, Jacqueline
Formato: Online Artículo Texto
Lenguaje:English
Publicado: MDPI 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9504780/
https://www.ncbi.nlm.nih.gov/pubmed/36144689
http://dx.doi.org/10.3390/molecules27185945
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author Stewart, Russell J.
Frandsen, Paul B.
Pauls, Steffen U.
Heckenhauer, Jacqueline
author_facet Stewart, Russell J.
Frandsen, Paul B.
Pauls, Steffen U.
Heckenhauer, Jacqueline
author_sort Stewart, Russell J.
collection PubMed
description The divergence of sister orders Trichoptera (caddisflies) and Lepidoptera (moths and butterflies) from a silk-spinning ancestor occurred around 290 million years ago. Trichoptera larvae are mainly aquatic, and Lepidoptera larvae are almost entirely terrestrial—distinct habitats that required molecular adaptation of their silk for deployment in water and air, respectively. The major protein components of their silks are heavy chain and light chain fibroins. In an effort to identify molecular changes in L-fibroins that may have contributed to the divergent use of silk in water and air, we used the ColabFold implementation of AlphaFold2 to predict three-dimensional structures of L-fibroins from both orders. A comparison of the structures revealed that despite the ancient divergence, profoundly different habitats, and low sequence conservation, a novel 10-helix core structure was strongly conserved in L-fibroins from both orders. Previously known intra- and intermolecular disulfide linkages were accurately predicted. Structural variations outside of the core may represent molecular changes that contributed to the evolution of insect silks adapted to water or air. The distributions of electrostatic potential, for example, were not conserved and present distinct order-specific surfaces for potential interactions with or modulation by external factors. Additionally, the interactions of L-fibroins with the H-fibroin C-termini are different for these orders; lepidopteran L-fibroins have N-terminal insertions that are not present in trichopteran L-fibroins, which form an unstructured ribbon in isolation but become part of an intermolecular β-sheet when folded with their corresponding H-fibroin C-termini. The results are an example of protein structure prediction from deep sequence data of understudied proteins made possible by AlphaFold2.
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spelling pubmed-95047802022-09-24 Conservation of Three-Dimensional Structure of Lepidoptera and Trichoptera L-Fibroins for 290 Million Years Stewart, Russell J. Frandsen, Paul B. Pauls, Steffen U. Heckenhauer, Jacqueline Molecules Article The divergence of sister orders Trichoptera (caddisflies) and Lepidoptera (moths and butterflies) from a silk-spinning ancestor occurred around 290 million years ago. Trichoptera larvae are mainly aquatic, and Lepidoptera larvae are almost entirely terrestrial—distinct habitats that required molecular adaptation of their silk for deployment in water and air, respectively. The major protein components of their silks are heavy chain and light chain fibroins. In an effort to identify molecular changes in L-fibroins that may have contributed to the divergent use of silk in water and air, we used the ColabFold implementation of AlphaFold2 to predict three-dimensional structures of L-fibroins from both orders. A comparison of the structures revealed that despite the ancient divergence, profoundly different habitats, and low sequence conservation, a novel 10-helix core structure was strongly conserved in L-fibroins from both orders. Previously known intra- and intermolecular disulfide linkages were accurately predicted. Structural variations outside of the core may represent molecular changes that contributed to the evolution of insect silks adapted to water or air. The distributions of electrostatic potential, for example, were not conserved and present distinct order-specific surfaces for potential interactions with or modulation by external factors. Additionally, the interactions of L-fibroins with the H-fibroin C-termini are different for these orders; lepidopteran L-fibroins have N-terminal insertions that are not present in trichopteran L-fibroins, which form an unstructured ribbon in isolation but become part of an intermolecular β-sheet when folded with their corresponding H-fibroin C-termini. The results are an example of protein structure prediction from deep sequence data of understudied proteins made possible by AlphaFold2. MDPI 2022-09-13 /pmc/articles/PMC9504780/ /pubmed/36144689 http://dx.doi.org/10.3390/molecules27185945 Text en © 2022 by the authors. https://creativecommons.org/licenses/by/4.0/Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
spellingShingle Article
Stewart, Russell J.
Frandsen, Paul B.
Pauls, Steffen U.
Heckenhauer, Jacqueline
Conservation of Three-Dimensional Structure of Lepidoptera and Trichoptera L-Fibroins for 290 Million Years
title Conservation of Three-Dimensional Structure of Lepidoptera and Trichoptera L-Fibroins for 290 Million Years
title_full Conservation of Three-Dimensional Structure of Lepidoptera and Trichoptera L-Fibroins for 290 Million Years
title_fullStr Conservation of Three-Dimensional Structure of Lepidoptera and Trichoptera L-Fibroins for 290 Million Years
title_full_unstemmed Conservation of Three-Dimensional Structure of Lepidoptera and Trichoptera L-Fibroins for 290 Million Years
title_short Conservation of Three-Dimensional Structure of Lepidoptera and Trichoptera L-Fibroins for 290 Million Years
title_sort conservation of three-dimensional structure of lepidoptera and trichoptera l-fibroins for 290 million years
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9504780/
https://www.ncbi.nlm.nih.gov/pubmed/36144689
http://dx.doi.org/10.3390/molecules27185945
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