Butterfly gyroid nanostructures as a time-frozen glimpse of intracellular membrane development

Science Advances
Bodo D WiltsG E Schröder-Turk

Abstract

The formation of the biophotonic gyroid material in butterfly wing scales is an exceptional feat of evolutionary engineering of functional nanostructures. It is hypothesized that this nanostructure forms by chitin polymerization inside a convoluted membrane of corresponding shape in the endoplasmic reticulum. However, this dynamic formation process, including whether membrane folding and chitin expression are simultaneous or sequential processes, cannot yet be elucidated by in vivo imaging. We report an unusual hierarchical ultrastructure in the butterfly Thecla opisena that, as a solid material, allows high-resolution three-dimensional microscopy. Rather than the conventional polycrystalline space-filling arrangement, a gyroid occurs in isolated facetted crystallites with a pronounced size gradient. When interpreted as a sequence of time-frozen snapshots of the morphogenesis, this arrangement provides insight into the formation mechanisms of the nanoporous gyroid material as well as of the intracellular organelle membrane that acts as the template.

References

Dec 1, 1993·International Journal of Biological Macromolecules·J F Revol, R H Marchessault
Nov 5, 1997·Current Opinion in Structural Biology·V Luzzati
Feb 19, 2002·Chemical Reviews·Mohan Srinivasarao
Aug 15, 2003·Nature·Pete Vukusic, J Roy Sambles
Aug 12, 2006·Science·Eric BetzigHarald F Hess
Jan 20, 2007·Science·Pete VukusicJoe Noyes
Jun 15, 2007·Journal of the Royal Society, Interface·K Michielsen, D G Stavenga
Dec 20, 2007·Arthropod Structure & Development·Marco A Giraldo, Doekele G Stavenga
Sep 4, 2008·Angewandte Chemie·Stephen T HydeDavide M Proserpio
Apr 8, 2009·International Review of Cell and Molecular Biology·Zakaria A AlmsherqiYuru Deng
Jul 25, 2009·Science·Vivek SharmaMohan Srinivasarao
Jun 16, 2010·Proceedings of the National Academy of Sciences of the United States of America·Vinodkumar SaranathanRichard O Prum
Jun 18, 2011·Advanced Materials·G E Schröder-TurkK Mecke
Oct 25, 2011·Advanced Materials·Silvia VignoliniUllrich Steiner
Sep 29, 2012·Proceedings of the National Academy of Sciences of the United States of America·Silvia VignoliniUllrich Steiner
Feb 4, 2014·Advanced Materials·Maik R J SchererUllrich Steiner
Jun 17, 2014·Developmental Biology·April DinwiddieNipam H Patel
Aug 6, 2014·Proceedings of the National Academy of Sciences of the United States of America·Bethany R WasikAntónia Monteiro
Apr 10, 2015·Chemical Society Reviews·Morgan StefikUllrich Steiner
Apr 23, 2015·Nature Communications·Radwanul Hasan SiddiqueHendrik Hölscher
May 6, 2015·Nano Letters·Vinodkumar SaranathanRichard O Prum
Oct 7, 2015·Proceedings of the National Academy of Sciences of the United States of America·Benjamin WinterErdmann Spiecker
Nov 18, 2015·Nature Communications·Davide DemurtasLaurent Sagalowicz
Jul 8, 2016·Science Advances·Zongsong GanMin Gu
Oct 30, 2016·Science·Jonathon Nixon-AbellJennifer Lippincott-Schwartz

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Citations

Jun 24, 2017·Advanced Materials·Bodo D WiltsAlessandro Sepe
Feb 24, 2018·Proceedings of the National Academy of Sciences of the United States of America·Villads Egede JohansenSilvia Vignolini
Feb 15, 2018·Bioinspiration & Biomimetics·Ramneet K NagiMichael H Bartl
Mar 9, 2018·Advanced Materials·Thomas B H SchroederMichael Mayer
Aug 24, 2018·Journal of Physics. Condensed Matter : an Institute of Physics Journal·Stephanie L Burg, Andrew J Parnell
Jun 22, 2018·Angewandte Chemie·Hanna M G BarrigaMolly M Stevens
May 29, 2018·Chemistry : a European Journal·Qingqing ShengShunai Che
May 21, 2019·Developmental Dynamics : an Official Publication of the American Association of Anatomists·Christopher R DayArnaud Martin
Jun 22, 2019·Advanced Materials·Raffaele MezzengaLaurent Sagalowicz
Nov 7, 2019·Proceedings of the National Academy of Sciences of the United States of America·Michael A KlattSalvatore Torquato
May 17, 2019·Integrative and Comparative Biology·Ainsley E SeagoVinod Kumar Saranathan
Sep 20, 2019·Science Advances·S EhrigJohn W C Dunlop
Feb 14, 2020·Nanotechnology·Biao WuGuolan Fu
Oct 2, 2020·Faraday Discussions·Sébastien R MouchetPete Vukusic
Mar 29, 2020·Science China Materials·Congcong CuiLu Han
May 21, 2019·Biomimetics·Olimpia D OnelliSilvia Vignolini
Aug 8, 2020·Faraday Discussions·PrimoŽ PirihGregor Belušič
May 12, 2018·Advanced Materials·Qingchen ShenTao Deng
Nov 27, 2019·The Journal of Experimental Biology·Cédric KilchoerBodo D Wilts
Feb 5, 2021·Current Opinion in Genetics & Development·Victoria J Lloyd, Nicola J Nadeau
Feb 16, 2021·Journal of the Mechanical Behavior of Biomedical Materials·Cambre N KellyKen Gall
Mar 16, 2021·Dalton Transactions : an International Journal of Inorganic Chemistry·Yan Yan LiXiao-Ping Zhou
Mar 17, 2021·Proceedings of the National Academy of Sciences of the United States of America·Xueyan FengEdwin L Thomas
Jun 2, 2021·Proceedings of the Institution of Mechanical Engineers. Part H, Journal of Engineering in Medicine·Yogesh TripathiAmba D Bhatt
Apr 23, 2021·Angewandte Chemie·Qingqing ShengLu Han
Jun 3, 2021·Proceedings of the National Academy of Sciences of the United States of America·Vinodkumar SaranathanRichard O Prum
Jul 1, 2021·Microscopy and Microanalysis : the Official Journal of Microscopy Society of America, Microbeam Analysis Society, Microscopical Society of Canada·Wenting MaoLu Han
Jul 31, 2021·Physical Review Letters·Michael A KlattSalvatore Torquato
Jul 20, 2021·Advanced Materials·Wanlu LiYu Shrike Zhang
Aug 20, 2021·Langmuir : the ACS Journal of Surfaces and Colloids·Hong-Kai LiuWei Wang
Jan 11, 2020·Accounts of Chemical Research·Sungmin HaKyoung Taek Kim

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Methods Mentioned

BETA
fluorescence microscopy
confocal
transmission electron microscopy
x-ray microscopy
light microscopy
x-ray
electron microscopy
light scattering
x-ray tomography

Software Mentioned

Matlab

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