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Published August 8, 2019 | Accepted Version + Submitted + Supplemental Material
Journal Article Open

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

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.

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.

Attached Files

Accepted Version - nihms-1531196.pdf

Submitted - 1812.09418.pdf

Submitted - 504456.full.pdf

Supplemental Material - 41586_2019_1447_MOESM10_ESM.mp4

Supplemental Material - 41586_2019_1447_MOESM11_ESM.m4v

Supplemental Material - 41586_2019_1447_MOESM12_ESM.m4v

Supplemental Material - 41586_2019_1447_MOESM13_ESM.m4v

Supplemental Material - 41586_2019_1447_MOESM14_ESM.m4v

Supplemental Material - 41586_2019_1447_MOESM15_ESM.mov

Supplemental Material - 41586_2019_1447_MOESM1_ESM.pdf

Supplemental Material - 41586_2019_1447_MOESM2_ESM.avi

Supplemental Material - 41586_2019_1447_MOESM3_ESM.avi

Supplemental Material - 41586_2019_1447_MOESM4_ESM.avi

Supplemental Material - 41586_2019_1447_MOESM5_ESM.m4v

Supplemental Material - 41586_2019_1447_MOESM6_ESM.avi

Supplemental Material - 41586_2019_1447_MOESM7_ESM.m4v

Supplemental Material - 41586_2019_1447_MOESM8_ESM.m4v

Supplemental Material - 41586_2019_1447_MOESM9_ESM.m4v

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Additional details

Created:
August 19, 2023
Modified:
October 20, 2023