Dynamic self-assembly of compartmentalized DNA nanotubes

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Abstract

Bottom-up synthetic biology aims to engineer artificial cells capable of responsive behaviors by using a minimal set of molecular components. An important challenge toward this goal is the development of programmable biomaterials that can provide active spatial organization in cell-sized compartments. Here, we demonstrate the dynamic self-assembly of nucleic acid (NA) nanotubes inside water-in-oil droplets. We develop methods to encapsulate and assemble different types of DNA nanotubes from programmable DNA monomers, and demonstrate temporal control of assembly via designed pathways of RNA production and degradation. We examine the dynamic response of encapsulated nanotube assembly and disassembly with the support of statistical analysis of droplet images. Our study provides a toolkit of methods and components to build increasingly complex and functional NA materials to mimic life-like functions in synthetic cells.

Abstract

A major goal in Engineering Biology and Materials Science is the development of active, autonomous scaffolds that mimic those present in biological cells. Here the authors report a toolkit for programming the dynamic behaviour of nucleic acid scaffolds in minimal cell-like compartments.

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Structural absorption by barbule microstructures of super black bird of paradise feathers

Dakota E. McCoy, Teresa J. Feo, Todd Alan Harvey … (2018)

Many studies have shown how pigments and internal nanostructures generate color in nature. External surface structures can also influence appearance, such as by causing multiple scattering of light (structural absorption) to produce a velvety, super black appearance. Here we show that feathers from five species of birds of paradise (Aves: Paradisaeidae) structurally absorb incident light to produce extremely low-reflectance, super black plumages. Directional reflectance of these feathers (0.05–0.31%) approaches that of man-made ultra-absorbent materials. SEM, nano-CT, and ray-tracing simulations show that super black feathers have titled arrays of highly modified barbules, which cause more multiple scattering, resulting in more structural absorption, than normal black feathers. Super black feathers have an extreme directional reflectance bias and appear darkest when viewed from the distal direction. We hypothesize that structurally absorbing, super black plumage evolved through sensory bias to enhance the perceived brilliance of adjacent color patches during courtship display.

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Folding DNA to create nanoscale shapes and patterns.

Paul W. K Rothemund (2006)

'Bottom-up fabrication', which exploits the intrinsic properties of atoms and molecules to direct their self-organization, is widely used to make relatively simple nanostructures. A key goal for this approach is to create nanostructures of high complexity, matching that routinely achieved by 'top-down' methods. The self-assembly of DNA molecules provides an attractive route towards this goal. Here I describe a simple method for folding long, single-stranded DNA molecules into arbitrary two-dimensional shapes. The design for a desired shape is made by raster-filling the shape with a 7-kilobase single-stranded scaffold and by choosing over 200 short oligonucleotide 'staple strands' to hold the scaffold in place. Once synthesized and mixed, the staple and scaffold strands self-assemble in a single step. The resulting DNA structures are roughly 100 nm in diameter and approximate desired shapes such as squares, disks and five-pointed stars with a spatial resolution of 6 nm. Because each oligonucleotide can serve as a 6-nm pixel, the structures can be programmed to bear complex patterns such as words and images on their surfaces. Finally, individual DNA structures can be programmed to form larger assemblies, including extended periodic lattices and a hexamer of triangles (which constitutes a 30-megadalton molecular complex).

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A vesicle bioreactor as a step toward an artificial cell assembly.

Vincent Noireaux, Albert Libchaber (2004)

An Escherichia coli cell-free expression system is encapsulated in a phospholipid vesicle to build a cell-like bioreactor. Large unilamellar vesicles containing extracts are produced in an oil-extract emulsion. To form a bilayer the vesicles are transferred into a feeding solution that contains ribonucleotides and amino acids. Transcription-translation of plasmid genes is isolated in the vesicles. Whereas in bulk solution expression of enhanced GFP stops after 2 h, inside the vesicle permeability of the membrane to the feeding solution prolongs the expression for up to 5 h. To solve the energy and material limitations and increase the capacity of the reactor, the alpha-hemolysin pore protein from Staphylococcus aureus is expressed inside the vesicle to create a selective permeability for nutrients. The reactor can then sustain expression for up to 4 days with a protein production of 30 muM after 4 days. Oxygen diffusion and osmotic pressure are critical parameters to maintain expression and avoid vesicle burst.

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Author and article information

Contributors

Elisa Franco:

ORCID: http://orcid.org/0000-0003-1103-2668

efranco@seas.ucla.edu

Journal

Journal ID (nlm-ta): Nat Commun

Journal ID (iso-abbrev): Nat Commun

Title: Nature Communications

Publisher: Nature Publishing Group UK (London )

ISSN (Electronic): 2041-1723

Publication date (Electronic): 11 June 2021

Publication date PMC-release: 11 June 2021

Publication date Collection: 2021

Volume: 12

Affiliations

[1 ]GRID grid.19006.3e, ISNI 0000 0000 9632 6718, Department of Bioengineering, University of California, ; Los Angeles, CA USA

[2 ]GRID grid.266097.c, ISNI 0000 0001 2222 1582, Department of Mechanical Engineering, University of California, ; Riverside, CA USA

[3 ]GRID grid.19006.3e, ISNI 0000 0000 9632 6718, Department of Mechanical and Aerospace Engineering, University of California, ; Los Angeles, CA USA

[4 ]GRID grid.19006.3e, ISNI 0000 0000 9632 6718, Molecular Biology Institute, University of California, ; Los Angeles, CA USA

Article

Publisher ID: 23850

DOI: 10.1038/s41467-021-23850-1

PMC ID: 8196065

PubMed ID: 34117248

SO-VID: 8c46e274-eb74-47d9-a690-9b11b01db492

License:

Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.

Funding

Funded by: FundRef https://doi.org/10.13039/100000015, U.S. Department of Energy (DOE);

Award ID: DE-SC-0010595

Award Recipient : Elisa Franco

Funded by: FundRef https://doi.org/10.13039/100000002, U.S. Department of Health & Human Services | National Institutes of Health (NIH);

Award ID: S10OD025017

Award Recipient : Elisa Franco

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ScienceOpen disciplines: Uncategorized

Keywords: synthetic biology,bioinspired materials,dna nanostructures,molecular self-assembly

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ScienceOpen disciplines: Uncategorized

Keywords: synthetic biology, bioinspired materials, dna nanostructures, molecular self-assembly

Dynamic self-assembly of compartmentalized DNA nanotubes

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Most cited references 80

Structural absorption by barbule microstructures of super black bird of paradise feathers

Folding DNA to create nanoscale shapes and patterns.

A vesicle bioreactor as a step toward an artificial cell assembly.

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