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Controlling Organization and Forces in Active Matter Through Optically-Defined Boundaries

Ross, Tyler D. and Lee, Heun Jin and Qu, Zijie and Banks, Rachel A. and Phillips, Rob and Thomson, Matt (2019) Controlling Organization and Forces in Active Matter Through Optically-Defined Boundaries. Nature, 572 (7768). pp. 224-229. ISSN 0028-0836. http://resolver.caltech.edu/CaltechAUTHORS:20190102-092232993

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Abstract

Living systems are capable of locomotion, reconfiguration and replication. To perform these tasks, cells spatiotemporally coordinate the interactions of force-generating, ‘active’ molecules that create and manipulate non-equilibrium structures and force fields of up to millimetre length scales. Experimental active-matter systems of biological or synthetic molecules are capable of spontaneously organizing into structures and generating global flows. However, these experimental systems lack the spatiotemporal control found in cells, limiting their utility for studying non-equilibrium phenomena and bioinspired engineering. Here we uncover non-equilibrium phenomena and principles of boundary-mediated control by optically modulating structures and fluid flow in an engineered system of active biomolecules. Our system consists of purified microtubules and light-activatable motor proteins that crosslink and organize the microtubules into distinct structures upon illumination. We develop basic operations—defined as sets of light patterns—to create, move and merge the microtubule structures. By combining these operations, we create microtubule networks that span several hundred micrometres in length and contract at speeds up to an order of magnitude higher than the speed of an individual motor protein. We manipulate these contractile networks to generate and sculpt persistent fluid flows. The principles of boundary-mediated control that we uncover may be used to study emergent cellular structures and forces and to develop programmable active-matter devices.


Item Type:Article
Related URLs:
URLURL TypeDescription
https://doi.org/10.1038/s41586-019-1447-1DOIArticle
https://rdcu.be/bNyFgPublisherFree ReadCube access
https://doi.org/10.1101/504456DOIDiscussion Paper
https://arxiv.org/abs/1812.09418arXivDiscussion Paper
https://data.caltech.edu/records/1160DOIData
ORCID:
AuthorORCID
Ross, Tyler D.0000-0002-7872-3992
Phillips, Rob0000-0003-3082-2809
Additional Information:© 2019 Springer Nature Publishing AG. Received 11 January 2019; Accepted 05 June 2019; Published 07 August 2019. Data availability: The data that support the findings of this study are available from the Caltech Research Data Repository at https://data.caltech.edu/records/1160. All plasmids used in this study are available at https://www.addgene.org. All of the other reagents and the source code used for this study are available from the corresponding authors upon reasonable request. We thank M. Anjur-Dietrich, J. Brady, J. Bruck, V. Galstyan, S. Hirokawa, C. Hueschen, Y. Lazebnik, W. Lim, W. Marshall, D. Mullins, D. Needleman, P. Rothemund and E. Winfree for scientific discussions. We thank L. Bugaj, Z. Dogic, A. Frost, W. Huynh, R. Ismagilov, L. Metcalf, H. Nguyen and R. Vale for advice and assistance during the development of the experimental system; K. van den Dries for assistance with three-dimensional visualization of asters; P. Sternberg for use of a microscopy system for initial light-activation experiments. We are grateful to N. Orme for assistance with figures and illustrations. We acknowledge support from the NIH through grants 1R35 GM118043-01 (R.P.) and NIH DP5 OD012194 (M.T.); the NSF through NSF 1330864 (M.T.); the John Templeton Foundation as part of the Boundaries of Life Initiative through grants 51250 & 60973 (R.P.); the Foundational Questions Institute and Fetzer Franklin Fund through FQXi 1816 (R.P., M.T.); and the UCSF Center for Systems and Synthetic Biology NIGMS P50 GM081879 (M.T.). M.T. acknowledges support from the Heritage Medical Research Institute. Author Contributions: T.D.R., H.J.L., R.P. and M.T. conceived the experiments and interpreted the results. T.D.R., H.J.L., R.A.B., Z.Q. and M.T. wrote the manuscript. T.D.R. designed and cloned iLID motor fusion constructs. T.D.R., H.J.L. and R.A.B. performed protein purification. T.D.R. and H.J.L. designed, performed and analysed the active-matter experiments. Z.Q. analysed and modelled flow data and tracked trajectories of moving asters. R.A.B. performed and analysed gliding assays. All authors discussed the results and commented on the manuscript. The authors declare no competing interests.
Group:Heritage Medical Research Institute
Funders:
Funding AgencyGrant Number
NIH1R35 GM118043-01
NIHDP5 OD012194
NSFMCB-1330864
John Templeton Foundation51250
John Templeton Foundation60973
Foundational Questions Institute (FQXI)FQXi-RFP-1816
NIHP50 GM081879
Heritage Medical Research InstituteUNSPECIFIED
Issue or Number:7768
Record Number:CaltechAUTHORS:20190102-092232993
Persistent URL:http://resolver.caltech.edu/CaltechAUTHORS:20190102-092232993
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:91968
Collection:CaltechAUTHORS
Deposited By: George Porter
Deposited On:02 Jan 2019 18:45
Last Modified:07 Aug 2019 21:34

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