Micro and nano-scale compartments guide the structural transition of silk protein monomers into silk fibers

D. Eliaz; S. Paul; D. Benyamin; A. Cernescu; S. R. Cohen; I. Rosenhek-Goldian; O. Brookstein; M. E. Miali; A. Solomonov; M. Greenblatt; Y. Levy; U. Raviv; A. Barth; U. Shimanovich

doi:10.1038/s41467-022-35505-w

Micro and nano-scale compartments guide the structural transition of silk protein monomers into silk fibers

D. Eliaz, S. Paul, D. Benyamin, A. Cernescu, S. R. Cohen, I. Rosenhek-Goldian, O. Brookstein, M. E. Miali, A. Solomonov, M. Greenblatt, Y. Levy, U. Raviv, A. Barth, U. Shimanovich

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51 Scopus citations

Abstract

Silk is a unique, remarkably strong biomaterial made of simple protein building blocks. To date, no synthetic method has come close to reproducing the properties of natural silk, due to the complexity and insufficient understanding of the mechanism of the silk fiber formation. Here, we use a combination of bulk analytical techniques and nanoscale analytical methods, including nano-infrared spectroscopy coupled with atomic force microscopy, to probe the structural characteristics directly, transitions, and evolution of the associated mechanical properties of silk protein species corresponding to the supramolecular phase states inside the silkworm’s silk gland. We found that the key step in silk-fiber production is the formation of nanoscale compartments that guide the structural transition of proteins from their native fold into crystalline β-sheets. Remarkably, this process is reversible. Such reversibility enables the remodeling of the final mechanical characteristics of silk materials. These results open a new route for tailoring silk processing for a wide range of new material formats by controlling the structural transitions and self-assembly of the silk protein’s supramolecular phases.

Original language	English
Article number	7856
Journal	Nature Communications
Volume	13
Issue number	1
DOIs	https://doi.org/10.1038/s41467-022-35505-w
State	Published - 21 Dec 2022
Externally published	Yes

Bibliographical note

Publisher Copyright:
© 2022, The Author(s).

Funding

We thank Prof. Gilad Haran and Prof. Jacob Klein for useful discussions and for comments on the manuscript. US acknowledges financial support from the Gruber Foundation, Nella and Leon Benoziyo Center for Neurological Diseases, Alon Fellowship (Israeli Council for Higher Education). In addition, US thanks the Perlman family for funding the Shimanovich Lab at the Weizmann Institute of Science: “This research was made possible in part by the generosity of the Harold Perlman Family”. The authors would like to acknowledge partial support from the GMJ Schmidt Minerva Center of Supramolecular Architectures at the Weizmann Institute. SP and AB are grateful to Olle Engkvist’s Foundation for financing the IR nanospectrometer and a project grant that included a postdoctoral fellowship. We thank the European Synchrotron Radiation Facility for providing access to their synchrotron radiation facilities, and we thank T. Narayanan and L. Matthews for assistance in using the SAXS setup at beamline ID02 and Daniel Khaykelson for the assistance in SAXS measurements. The authors are grateful to Natalie Page for editing the manuscript.

Funders
Olle Engkvist’s Foundation
Perlman family for funding the Shimanovich Lab
Gruber Foundation
Weizmann Institute of Science
Council for Higher Education

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Eliaz, D., Paul, S., Benyamin, D., Cernescu, A., Cohen, S. R., Rosenhek-Goldian, I., Brookstein, O., Miali, M. E., Solomonov, A., Greenblatt, M., Levy, Y., Raviv, U., Barth, A., & Shimanovich, U. (2022). Micro and nano-scale compartments guide the structural transition of silk protein monomers into silk fibers. Nature Communications, 13(1), Article 7856. https://doi.org/10.1038/s41467-022-35505-w

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abstract = "Silk is a unique, remarkably strong biomaterial made of simple protein building blocks. To date, no synthetic method has come close to reproducing the properties of natural silk, due to the complexity and insufficient understanding of the mechanism of the silk fiber formation. Here, we use a combination of bulk analytical techniques and nanoscale analytical methods, including nano-infrared spectroscopy coupled with atomic force microscopy, to probe the structural characteristics directly, transitions, and evolution of the associated mechanical properties of silk protein species corresponding to the supramolecular phase states inside the silkworm{\textquoteright}s silk gland. We found that the key step in silk-fiber production is the formation of nanoscale compartments that guide the structural transition of proteins from their native fold into crystalline β-sheets. Remarkably, this process is reversible. Such reversibility enables the remodeling of the final mechanical characteristics of silk materials. These results open a new route for tailoring silk processing for a wide range of new material formats by controlling the structural transitions and self-assembly of the silk protein{\textquoteright}s supramolecular phases.",

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Eliaz, D, Paul, S, Benyamin, D, Cernescu, A, Cohen, SR, Rosenhek-Goldian, I, Brookstein, O, Miali, ME, Solomonov, A, Greenblatt, M, Levy, Y, Raviv, U, Barth, A & Shimanovich, U 2022, 'Micro and nano-scale compartments guide the structural transition of silk protein monomers into silk fibers', Nature Communications, vol. 13, no. 1, 7856. https://doi.org/10.1038/s41467-022-35505-w

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AU - Eliaz, D.

AU - Paul, S.

AU - Benyamin, D.

AU - Cernescu, A.

AU - Cohen, S. R.

AU - Rosenhek-Goldian, I.

AU - Brookstein, O.

AU - Miali, M. E.

AU - Solomonov, A.

AU - Greenblatt, M.

AU - Levy, Y.

AU - Raviv, U.

AU - Barth, A.

AU - Shimanovich, U.

PY - 2022/12/21

Y1 - 2022/12/21

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AB - Silk is a unique, remarkably strong biomaterial made of simple protein building blocks. To date, no synthetic method has come close to reproducing the properties of natural silk, due to the complexity and insufficient understanding of the mechanism of the silk fiber formation. Here, we use a combination of bulk analytical techniques and nanoscale analytical methods, including nano-infrared spectroscopy coupled with atomic force microscopy, to probe the structural characteristics directly, transitions, and evolution of the associated mechanical properties of silk protein species corresponding to the supramolecular phase states inside the silkworm’s silk gland. We found that the key step in silk-fiber production is the formation of nanoscale compartments that guide the structural transition of proteins from their native fold into crystalline β-sheets. Remarkably, this process is reversible. Such reversibility enables the remodeling of the final mechanical characteristics of silk materials. These results open a new route for tailoring silk processing for a wide range of new material formats by controlling the structural transitions and self-assembly of the silk protein’s supramolecular phases.

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Micro and nano-scale compartments guide the structural transition of silk protein monomers into silk fibers

Abstract

Bibliographical note

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