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Gradients of orientation, composition and hydration of proteins for efficient light collection by the cornea of the horseshoe crab

View ORCID ProfileOliver Spaeker, View ORCID ProfileGavin Taylor, View ORCID ProfileBodo Wilts, Tomáš Slabý, Mohamed Ashraf Khalil Abdel-Rahman, View ORCID ProfileErnesto Scoppola, View ORCID ProfileClemens NZ Schmitt, View ORCID ProfileMichael Sztucki, View ORCID ProfileJiliang Liu, View ORCID ProfileLuca Bertinetti, View ORCID ProfileWolfgang Wagermaier, View ORCID ProfileGerhard Scholtz, View ORCID ProfilePeter Fratzl, View ORCID ProfileYael Politi
doi: https://doi.org/10.1101/2022.02.21.481013
Oliver Spaeker
1Department of Biomaterials, Max Planck Institute of Colloids and Interfaces, 14476 Potsdam, Germany
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Gavin Taylor
2Institute for Globally Distributed Open Research and Education (IGDORE), Ribeirão Preto, 14091-310, Brazil
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Bodo Wilts
3Chemistry and Physics of Materials, University of Salzburg, Jakob-Haringer-Str. 2a, 5020 Salzburg, Austria
4Adolphe Merkle Institute, University of Fribourg, Chemin des Verdiers 4, 1700 Fribourg, Switzerland
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Tomáš Slabý
5TELIGHT, Libušina třída 21, Brno 623 00, Czech Republic
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Mohamed Ashraf Khalil Abdel-Rahman
5TELIGHT, Libušina třída 21, Brno 623 00, Czech Republic
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Ernesto Scoppola
1Department of Biomaterials, Max Planck Institute of Colloids and Interfaces, 14476 Potsdam, Germany
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Clemens NZ Schmitt
1Department of Biomaterials, Max Planck Institute of Colloids and Interfaces, 14476 Potsdam, Germany
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Michael Sztucki
6European Synchrotron Radiation Facility (ESRF) 71, avenue des Martyrs, CS 40220, Grenoble Cedex 9 38043, France
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Jiliang Liu
6European Synchrotron Radiation Facility (ESRF) 71, avenue des Martyrs, CS 40220, Grenoble Cedex 9 38043, France
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Luca Bertinetti
7B CUBE - Center for Molecular Bioengineering, Technische Universität Dresden, 01307 Dresden, Germany
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Wolfgang Wagermaier
1Department of Biomaterials, Max Planck Institute of Colloids and Interfaces, 14476 Potsdam, Germany
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Gerhard Scholtz
8Humboldt-University Berlin, Institute of Biology, Philippstraße 13, 10115 Berlin, Germany
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Peter Fratzl
1Department of Biomaterials, Max Planck Institute of Colloids and Interfaces, 14476 Potsdam, Germany
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Yael Politi
7B CUBE - Center for Molecular Bioengineering, Technische Universität Dresden, 01307 Dresden, Germany
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  • For correspondence: yael.politi@tu-dresden.de
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Abstract

The lateral eyes of the horseshoe crab, Limulus polyphemus, are the largest compound eyes within recent Arthropoda. While this visual system has been extensively described before, the precise mechanism allowing vision has remained controversial. Correlating quantitative refractive index (RI) mapping and detailed structural analysis, we demonstrate how gradients of RI in the cornea result from the hierarchical organization of chitin-protein fibers, heterogeneity in protein composition and bromine doping, as well as spatial variation in water content. Combining the realistic cornea structure and measured RI gradients with full-wave optical modelling and ray-tracing approaches, we show that the light collection mechanism depends on both refraction-based graded index (GRIN) optics and total internal reflection. The optical properties of the cornea are governed by different mechanisms at different hierarchical levels, demonstrating the remarkable versatility of arthropod cuticle.

One-sentence summary Structural hierarchy and protein hydration determine the optical performance of the cornea of L. polyphemus.

Competing Interest Statement

TS and MAKAR are employed by TELIGHT. All other authors declare that they have no competing interests.

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY 4.0 International license.
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Posted February 21, 2022.
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Gradients of orientation, composition and hydration of proteins for efficient light collection by the cornea of the horseshoe crab
Oliver Spaeker, Gavin Taylor, Bodo Wilts, Tomáš Slabý, Mohamed Ashraf Khalil Abdel-Rahman, Ernesto Scoppola, Clemens NZ Schmitt, Michael Sztucki, Jiliang Liu, Luca Bertinetti, Wolfgang Wagermaier, Gerhard Scholtz, Peter Fratzl, Yael Politi
bioRxiv 2022.02.21.481013; doi: https://doi.org/10.1101/2022.02.21.481013
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Gradients of orientation, composition and hydration of proteins for efficient light collection by the cornea of the horseshoe crab
Oliver Spaeker, Gavin Taylor, Bodo Wilts, Tomáš Slabý, Mohamed Ashraf Khalil Abdel-Rahman, Ernesto Scoppola, Clemens NZ Schmitt, Michael Sztucki, Jiliang Liu, Luca Bertinetti, Wolfgang Wagermaier, Gerhard Scholtz, Peter Fratzl, Yael Politi
bioRxiv 2022.02.21.481013; doi: https://doi.org/10.1101/2022.02.21.481013

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