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A fast recoiling silk-like elastomer facilitates nanosecond nematocyst discharge

BACKGROUND: The discharge of the Cnidarian stinging organelle, the nematocyst, is one of the fastest processes in biology and involves volume changes of the highly pressurised (150 bar) capsule of up to 50%. Hitherto, the molecular basis for the unusual biomechanical properties of nematocysts has be...

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Autores principales: Beckmann, Anna, Xiao, Senbo, Müller, Jochen P, Mercadante, Davide, Nüchter, Timm, Kröger, Niels, Langhojer, Florian, Petrich, Wolfgang, Holstein, Thomas W, Benoit, Martin, Gräter, Frauke, Özbek, Suat
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2015
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4321713/
https://www.ncbi.nlm.nih.gov/pubmed/25592740
http://dx.doi.org/10.1186/s12915-014-0113-1
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author Beckmann, Anna
Xiao, Senbo
Müller, Jochen P
Mercadante, Davide
Nüchter, Timm
Kröger, Niels
Langhojer, Florian
Petrich, Wolfgang
Holstein, Thomas W
Benoit, Martin
Gräter, Frauke
Özbek, Suat
author_facet Beckmann, Anna
Xiao, Senbo
Müller, Jochen P
Mercadante, Davide
Nüchter, Timm
Kröger, Niels
Langhojer, Florian
Petrich, Wolfgang
Holstein, Thomas W
Benoit, Martin
Gräter, Frauke
Özbek, Suat
author_sort Beckmann, Anna
collection PubMed
description BACKGROUND: The discharge of the Cnidarian stinging organelle, the nematocyst, is one of the fastest processes in biology and involves volume changes of the highly pressurised (150 bar) capsule of up to 50%. Hitherto, the molecular basis for the unusual biomechanical properties of nematocysts has been elusive, as their structure was mainly defined as a stress-resistant collagenous matrix. RESULTS: Here, we characterise Cnidoin, a novel elastic protein identified as a structural component of Hydra nematocysts. Cnidoin is expressed in nematocytes of all types and immunostainings revealed incorporation into capsule walls and tubules concomitant with minicollagens. Similar to spider silk proteins, to which it is related at sequence level, Cnidoin possesses high elasticity and fast coiling propensity as predicted by molecular dynamics simulations and quantified by force spectroscopy. Recombinant Cnidoin showed a high tendency for spontaneous aggregation to bundles of fibrillar structures. CONCLUSIONS: Cnidoin represents the molecular factor involved in kinetic energy storage and release during the ultra-fast nematocyst discharge. Furthermore, it implies an early evolutionary origin of protein elastomers in basal metazoans. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12915-014-0113-1) contains supplementary material, which is available to authorized users.
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spelling pubmed-43217132015-02-10 A fast recoiling silk-like elastomer facilitates nanosecond nematocyst discharge Beckmann, Anna Xiao, Senbo Müller, Jochen P Mercadante, Davide Nüchter, Timm Kröger, Niels Langhojer, Florian Petrich, Wolfgang Holstein, Thomas W Benoit, Martin Gräter, Frauke Özbek, Suat BMC Biol Research Article BACKGROUND: The discharge of the Cnidarian stinging organelle, the nematocyst, is one of the fastest processes in biology and involves volume changes of the highly pressurised (150 bar) capsule of up to 50%. Hitherto, the molecular basis for the unusual biomechanical properties of nematocysts has been elusive, as their structure was mainly defined as a stress-resistant collagenous matrix. RESULTS: Here, we characterise Cnidoin, a novel elastic protein identified as a structural component of Hydra nematocysts. Cnidoin is expressed in nematocytes of all types and immunostainings revealed incorporation into capsule walls and tubules concomitant with minicollagens. Similar to spider silk proteins, to which it is related at sequence level, Cnidoin possesses high elasticity and fast coiling propensity as predicted by molecular dynamics simulations and quantified by force spectroscopy. Recombinant Cnidoin showed a high tendency for spontaneous aggregation to bundles of fibrillar structures. CONCLUSIONS: Cnidoin represents the molecular factor involved in kinetic energy storage and release during the ultra-fast nematocyst discharge. Furthermore, it implies an early evolutionary origin of protein elastomers in basal metazoans. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12915-014-0113-1) contains supplementary material, which is available to authorized users. BioMed Central 2015-01-16 /pmc/articles/PMC4321713/ /pubmed/25592740 http://dx.doi.org/10.1186/s12915-014-0113-1 Text en © Beckmann et al.; licensee BioMed Central. 2015 This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. 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.
spellingShingle Research Article
Beckmann, Anna
Xiao, Senbo
Müller, Jochen P
Mercadante, Davide
Nüchter, Timm
Kröger, Niels
Langhojer, Florian
Petrich, Wolfgang
Holstein, Thomas W
Benoit, Martin
Gräter, Frauke
Özbek, Suat
A fast recoiling silk-like elastomer facilitates nanosecond nematocyst discharge
title A fast recoiling silk-like elastomer facilitates nanosecond nematocyst discharge
title_full A fast recoiling silk-like elastomer facilitates nanosecond nematocyst discharge
title_fullStr A fast recoiling silk-like elastomer facilitates nanosecond nematocyst discharge
title_full_unstemmed A fast recoiling silk-like elastomer facilitates nanosecond nematocyst discharge
title_short A fast recoiling silk-like elastomer facilitates nanosecond nematocyst discharge
title_sort fast recoiling silk-like elastomer facilitates nanosecond nematocyst discharge
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4321713/
https://www.ncbi.nlm.nih.gov/pubmed/25592740
http://dx.doi.org/10.1186/s12915-014-0113-1
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