Topologically-guided continuous protein crystallization controls bacterial surface layer self-assembly

Comerci, Colin J.; Herrmann, Jonathan; Yoon, Joshua; Jabbarpour, Fatemeh; Zhou, Xiaofeng; Nomellini, John F.; Smit, John; Shapiro, Lucy; Wakatsuki, Soichi; Moerner, W. E.

doi:10.1038/s41467-019-10650-x

Title: Topologically-guided continuous protein crystallization controls bacterial surface layer self-assembly

Journal Article · 21 June 2019 · Nature Communications

DOI: https://doi.org/10.1038/s41467-019-10650-x · OSTI ID:1619527

Comerci, Colin J. ^[1]; Herrmann, Jonathan ^[2]; Yoon, Joshua ^[1]; Jabbarpour, Fatemeh ^[2]; Zhou, Xiaofeng ^[1]; Nomellini, John F. ^[3];

^[3]; Shapiro, Lucy ^[1];

^[2];

^[1]

Stanford Univ., CA (United States)
Stanford Univ., CA (United States); SLAC National Accelerator Lab., Menlo Park, CA (United States)
Univ. of British Columbia, Vancouver, BC (Canada)

Many bacteria and most archaea possess a crystalline protein surface layer (S-layer), which surrounds their growing and topologically complicated outer surface. Constructing a macromolecular structure of this scale generally requires localized enzymatic machinery, but a regulatory framework for S-layer assembly has not been identified. By labeling, superresolution imaging, and tracking the S-layer protein (SLP) from C. crescentus, we show that 2D protein self-assembly is sufficient to build and maintain the S-layer in living cells by efficient protein crystal nucleation and growth. We propose a model supported by single-molecule tracking whereby randomly secreted SLP monomers diffuse on the lipopolysaccharide (LPS) outer membrane until incorporated at the edges of growing 2D S-layer crystals. Surface topology creates crystal defects and boundaries, thereby guiding S-layer assembly. Unsupervised assembly poses challenges for therapeutics targeting S-layers. However, protein crystallization as an evolutionary driver rationalizes S-layer diversity and raises the potential for biologically inspired self-assembling macromolecular nanomaterials.

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Research Organization:: SLAC National Accelerator Laboratory (SLAC), Menlo Park, CA (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER); USDOE

Grant/Contract Number:: AC02-76SF00515; R35-GM118067; R35-GM118071

OSTI ID:: 1619527

Alternate ID(s):: OSTI ID: 1546945; OSTI ID: 1608960

Journal Information:: Nature Communications, Vol. 10, Issue 1; ISSN 2041-1723

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United States

Language:: English

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A bacterial surface layer protein exploits multistep crystallization for rapid self-assembly Herrmann, Jonathan; Li, Po-Nan; Jabbarpour, Fatemeh Proceedings of the National Academy of Sciences, Vol. 117, Issue 1 https://doi.org/10.1073/pnas.1909798116	journal	December 2019
A bacterial surface layer protein exploits multistep crystallization for rapid self-assembly Herrmann, Jonathan; Li, Po-Nan; Jabbarpour, Fatemeh Proceedings of the National Academy of Sciences, Vol. 117, Issue 1 https://doi.org/10.1073/pnas.1909798116	journal	December 2019

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