Chromatographic separation of active polymer–like worm mixtures by contour length and activity
A unique way to sort mixtures of active polymers on the basis of their length and activity is demonstrated.
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Chromatographic separation of active polymer–like worm mixtures by contour length and activity
Abstract
The convective transport rate of polymers through confined geometries depends on their size, allowing for size-based separation of polymer mixtures (chromatography). Here, we investigate whether mixtures of active polymers can be separated in a similar manner based on their activity. We use thin, living
Tubifex tubifex
worms as a model system for active polymers and study the transport of these worms by an imposed flow through a channel filled with a hexagonal pillar array. The transport rate through the channel depends strongly on the degree of activity, an effect that we assign to the different distribution of conformations sampled by the worms depending on their activity. Our results demonstrate a unique way to sort mixtures of active polymers based on their activity and provide a versatile and convenient experimental system to investigate the hydrodynamics of active polymers.
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REFERENCES AND NOTES
1
M. C. Marchetti, J. F. Joanny, S. Ramaswamy, T. B. Liverpool, J. Prost, M. Rao, R. A. Simha, Hydrodynamics of soft active matter.
Phys. Rev. Lett.
85
, 1143–1189 (2013).
2
G. Salbreux, G. Charras, E. Paluch, Actin cortex mechanics and cellular morphogenesis.
Trends Cell Biol.
22
, 536–545 (2012).
3
D. A. Fletcher, P. L. Geissler, Active biological materials.
Annu. Rev. Phys. Chem.
60
, 469–486 (2009).
4
G. Vizsnyiczai, G. Frangipane, C. Maggi, F. Saglimbeni, S. Bianchi, R. Di Leonardo, Light controlled 3D micromotors powered by bacteria.
Nat. Commun.
8
, 15974 (2017).
5
L. Soler, V. Magdanz, V. M. Fomin, S. Sanchez, O. G. Schmidt, Self-propelled micromotors for cleaning polluted water.
ACS Nano
7
, 9611–9620 (2013).
6
A. Deblais, T. Barois, T. Guerin, P.-H. Delville, R. Vaudaine, J. S. Lintuvuori, J.-F. Boudet, J.-C. Baret, H. Kellay, Boundaries control collective dynamics of inertial self-propelled robots.
Phys. Rev. Lett.
120
, 188002 (2018).
7
W. Savoie, T. A. Berrueta, Z. Jackson, A. Pervan, R. Warkentin, S. Li, T. D. Murphey, K. Wiesenfeld, D. I. Goldman, A robot made of robots: Emergent transport and control of a smarticle ensemble.
Sci. Robot.
4
, eaax4316 (2019).
8
M. Guentzel, L. Berry, Motility as a virulence factor for vibrio cholerae.
Infect. Immun.
11
, 890–897 (1975).
9
G. Jones, L. A. Richardson, D. Uhlman, The invasion of HeLa cells by Salmonella typhimurium: Reversible and irreversible bacterial attachment and the role of bacterial motility.
J. Gen. Microbiology
127
, 351–360 (1981).
10
S. Nakao, T. Takeo, H. Watanabe, G. Kondoh, N. Nakagata, Successful selection of mouse sperm with high viability and fertility using microfluidics chip cell sorter.
Sci. Rep.
10
, 8862 (2020).
11
P. Denissenko, V. Kantsler, D. J. Smith, J. Kirkman-Brown, Human spermatozoa migration in microchannels reveals boundary-following navigation.
Proc. Natl. Acad. Sci. U.S.A.
109
, 8007–8010 (2012).
12
I. Berdakin, Y. Jeyaram, V. V. Moshchalkov, L. Venken, S. Dierckx, S. J. Vanderleyden, A. V. Silhanek, C. A. Condat, V. I. Marconi, Influence of swimming strategy on microorganism separation by asymmetric obstacles.
Phys. Rev. E
87
, 052702 (2013).
13
A. Costanzo, J. Elgeti, T. Auth, G. Gompper, M. Ripoll, Motility-sorting of self-propelled particles in microchannels.
Europhys. Lett.
107
, 36003 (2014).
14
T. Ostapenko, F. J. Schwarzendahl, T. J. Böddeker, C. T. Kreis, J. Cammann, M. G. Mazza, O. Bäumchen, Curvature-guided motility of microalgae in geometric confinement.
Phys. Rev. Lett.
120
, 068002 (2018).
15
R. Alonso-Matilla, B. Chakrabarti, D. Saintillan, Transport and dispersion of active particles in periodic porous media.
Phys. Rev. Fluids
4
, 043101 (2019).
16
T. Barois, J.-F. Boudet, J. S. Lintuvuori, H. Kellay, Sorting and extraction of self-propelled chiral particles by polarized wall currents.
Phys. Rev. Lett.
125
, 238003 (2020).
17
C. Maggi, A. Lepore, J. Solari, A. Rizzo, R. Di Leonardo, Motility fractionation of bacteria by centrifugation.
Soft Matter
9
, 10885 (2013).
18
O. Chepizhko, F. Peruani, Diffusion, subdiffusion, and trapping of active particles in heterogeneous media.
Phys. Rev. Lett.
111
, 160604 (2013).
19
C. Bechinger, R. Di Leonardo, H. Löwen, C. Reichhardt, G. Volpe, G. Volpe, Active particles in complex and crowded environments.
Rev. Mod. Phys.
88
, 045006 (2016).
20
A. Morin, D. L. Cardozo, V. Chikkadi, D. Bartolo, Diffusion, subdiffusion, and localization of active colloids in random post lattices.
Phys. Rev. E
96
, 042611 (2017).
21
A. Morin, N. Desreumaux, J.-B. Caussin, D. Bartolo, Distortion and destruction of colloidal flocks in disordered environments.
Nat. Phys.
13
, 63–67 (2017).
22
A. Chamolly, T. Ishikawa, E. Lauga, Active particles in periodic lattices.
New J. Phys.
19
, 115001 (2017).
23
A. Loisy, J. Eggers, T. B. Liverpool, Active suspensions have nonmonotonic flow curves and multiple mechanical equilibria.
Phys. Rev. Lett.
121
, 018001 (2018).
24
A. Creppy, E. Clément, C. Douarche, M. V. d’Angelo, H. Auradou, Effect of motility on the transport of bacteria populations through a porous medium.
Phys. Rev. Fluids
4
, 013102 (2019).
25
R. G. Winkler, G. Gompper, The physics of active polymers and filaments.
J. Chem. Phys.
153
, 040901 (2020).
26
R. G. Winkler, J. Elgeti, G. Gompper, Active polymers—Emergent conformational and dynamical properties: A brief review.
J. Physical Soc. Japan
86
, 101014 (2017).
27
S. Stuij, J. M. van Doorn, T. Kodger, J. Sprakel, C. Coulais, P. Schall, Stochastic buckling of self-assembled colloidal structures.
Phys. Rev. Res.
1
, 023033 (2019).
28
D. A. Gagnon, P. E. Arratia, The cost of swimming in generalized Newtonian fluids: Experiments with C. elegans.
J. Fluid Mech.
800
, 753–765 (2016).
29
A. Martín-Gómez, G. Gompper, R. G. Winkler, Active Brownian filamentous polymers under shear flow.
Polymers
10
, 837 (2018).
30
V. Bianco, E. Locatelli, P. Malgaretti, Globulelike conformation and enhanced diffusion of active polymers.
Phys. Rev. Lett.
121
, 217802 (2018).
31
A. Martín-Gómez, T. Eisenstecken, G. Gompper, R. G. Winkler, Active Brownian filaments with hydrodynamic interactions: Conformations and dynamics.
Soft Matter
15
, 3957–3969 (2019).
32
A. Deblais, S. Woutersen, D. Bonn, Rheology of entangled active polymer-like
T. Tubifex
worms.
Phys. Rev. Lett.
124
, 188002 (2020).
33
V. Schaller, C. Weber, C. Semmrich, E. Frey, A. R. Bausch, Polar patterns of driven filaments.
Nature
467
, 73–77 (2010).
34
A. Deblais, A. C. Maggs, D. Bonn, S. Woutersen, Phase separation by entanglement of active polymerlike worms.
Phys. Rev. Lett.
124
, 208006 (2020).
35
Z. Mokhtari, A. Zippelius, Dynamics of active filaments in porous media.
Phys. Rev. Lett.
123
, 028001 (2019).
36
S. Mandal, C. Kurzthaler, T. Franosch, H. Löwen, Crowding-enhanced diffusion: An exact theory for highly entangled self-propelled stiff filaments.
Phys. Rev. Lett.
125
, 138002 (2020).
37
Y. Ozkan-Aydin, D. I. Goldman, M. S. Bhamla, Collective dynamics in entangled worm and robot blobs.
Proc. Natl. Acad. Sci. U.S.A.
118
, 138002 (2021).
38
M. C. VandeSande, D. J. Pasut, H. W. de Haan, Sorting polymers by size via an array of viscous posts.
Electrophoresis
38
, 2488–2497 (2017).
39
D. Berek, Size exclusion chromatography—A blessing and a curse of science and technology of synthetic polymers.
J. Sep. Sci.
33
, 315–335 (2010).
40
M. Gaborieau, P. Castignolles, Size-exclusion chromatography (SEC) of branched polymers and polysaccharides.
Anal. Bioanal. Chem.
399
, 1413–1423 (2011).
41
A. M. Striegel, A. K. Brewer, Hydrodynamic chromatography.
Annu. Rev. Anal. Chem.
5
, 15–34 (2012).
42
P. Gzil, N. Vervoort, G. Baron, G. Desmet, Advantages of perfectly ordered 2-D porous pillar arrays over packed bed columns for LC separations: A theoretical analysis.
Anal. Chem.
75
, 6244–6250 (2003).
43
M. D. Pra, W. D. Malsche, G. Desmet, P. J. Schoenmakers, W. T. Kok, Pillar-structured microchannels for on-chip liquid chromatography: Evaluation of the permeability and separation performance.
J. Sep. Sci.
30
, 1453–1460 (2007).
44
J. O. De Beeck, W. De Malsche, J. Vangelooven, H. Gardeniers, G. Desmet, Hydrodynamic chromatography of polystyrene microparticles in micropillar array columns.
J. Chromatogr. A
1217
, 6077–6084 (2010).
45
A. Daneyko, S. Khirevich, A. Höltzel, A. Seidel-Morgenstern, U. Tallarek, From random sphere packings to regular pillar arrays: Effect of the macroscopic confinement on hydrodynamic dispersion.
J. Chromatogr. A
1218
, 8231–8248 (2011).
46
J. Hirabayashi, K. Kasai, Slalom chromatography. A new size-dependent separation method for DNA.
Nucleic Acid Symp. Ser.
20
, 67–68 (1988).
47
B. E. Boyes, D. G. Walker, P. L. McGeer, Separation of large DNA restriction fragments on a size-exclusion column by a nonideal mechanism.
Anal. Biochem.
170
, 127–134 (1988).
48
J. Hirabayashi, K.-i. Kasai, Slalom chromatography, in
Molecular Interactions in Bioseparations
(Springer, 1993), pp. 69–87.
49
I. Teraoka,
Polymer Solutions
(John Wiley & Sons, Inc., 2002).
50
C. P. Brangwynne, G. H. Koenderink, E. Barry, Z. Dogic, F. C. MacKintosh, D. A. Weitz, Bending dynamics of fluctuating biopolymers probed by automated highresolution filament tracking.
Biophys. J.
93
, 346–359 (2007).
51
G. Lamour, J. B. Kirkegaard, H. Li, T. P. Knowles, J. Gsponer, Easyworm: An open-source software tool to determine the mechanical properties of worm-like chains.
Source Code Biol. Med.
9
, 16 (2014).
52
F. Gittes, B. Mickey, J. Nettleton, J. Howard, Flexural rigidity of microtubules and actin filaments measured from thermal fluctuations in shape.
J. Cell Biol.
120
, 923–934 (1993).
53
E. Uliyanchenko, S. van der Wal, P. J. Schoenmakers, Challenges in polymer analysis by liquid chromatography.
Polym. Chem.
3
, 2313 (2012).
54
J. Hirabayashi, N. Ito, K. Noguchi, K. Kasai, Slalom chromatography: Size-dependent separation of DNA molecules by a hydrodynamic phenomenon.
Biochemistry
29
, 9515–9521 (1990).
55
S. Mori, H. G. Barth,
Size Exclusion Chromatography
(Springer Science & Business Media, 2013).
56
B. Chakrabarti, C. Gaillard, D. Saintillan, Trapping, gliding, vaulting: Transport of semiflexible polymers in periodic post arrays.
Soft Matter
16
, 5534–5544 (2020).
57
R. Chelakkot, R. G. Winkler, G. Gompper, Flow-induced helical coiling of semiflexible polymers in structured microchannels.
Phys. Rev. Lett.
109
, 178101 (2012).
58
B. Chakrabarti, Y. Liu, J. LaGrone, R. Cortez, L. Fauci, O. Du Roure, D. Saintillan, A. Lindner, Flexible filaments buckle into helicoidal shapes in strong compressional flows.
Nat. Phys.
16
, 689–694 (2020).
59
E. Wandersman, N. Quennouz, M. Fermigier, A. Lindner, O. Du Roure, Buckled in translation.
Soft Matter
6
, 5715 (2010).
60
C. Kurzthaler, Elastic behavior of a semiflexible polymer in 3D subject to compression and stretching forces.
Soft Matter
14
, 7634–7644 (2018).
61
O. Du Roure, A. Lindner, E. N. Nazockdast, M. J. Shelley, Dynamics of flexible fibers in viscous flows and fluids.
Annu. Rev. Fluid Mech.
51
, 539–572 (2019).
62
P. J. Żuk, A. M. Słowicka, M. L. Ekiel-Jeżewska, H. A. Stone, Universal features of the shape of elastic fibres in shear flow.
J. Fluid Mech.
914
, A31 (2021).
63
J. C. Crocker, D. G. Grier, Methods of digital video microscopy for colloidal studies.
J. Colloid Interface Sci.
179
, 298–310 (1996).
Information & Authors
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Published In
Science Advances
Volume
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Issue
23
June 2022
June 2022
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Copyright © 2022 The Authors, some rights reserved; exclusive licensee American Association for the Advancement of Science. No claim to original U.S. Government Works. Distributed under a Creative Commons Attribution NonCommercial License 4.0 (CC BY-NC).
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Submission history
Received
: 4 June 2021
Accepted
: 20 April 2022
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Acknowledgments
We thank B. Pirok and P. Schoenmakers for fruitful discussions, the UvA’s workshop for technical assistance, and aquarium shop Rainer for the fresh batches of
T. tubifex
.
Funding:
The authors acknowledge that they received no funding in support of this research.
Author contributions:
T.H., A.D., and S.W. designed the research, and T.H. built the experimental setup with the help of the workshop of the University of Amsterdam; T.H. and A.D. performed the research; T.H. analyzed the data; and all the authors contributed to the final version of the manuscript.
Competing interests:
The authors declare that they have no competing interests.
Data and materials availability:
All data needed to evaluate the conclusions in the paper are present in the paper and/or the Supplementary Materials.
Authors
Affiliations
Van der Waals-Zeeman Institute, IoP, University of Amsterdam, Science Park 904, 1098 XH, Amsterdam, Netherlands.
Van der Waals-Zeeman Institute, IoP, University of Amsterdam, Science Park 904, 1098 XH, Amsterdam, Netherlands.
Van der Waals-Zeeman Institute, IoP, University of Amsterdam, Science Park 904, 1098 XH, Amsterdam, Netherlands.
Van ’t Hoff Institute for Molecular Sciences, University of Amsterdam, Science Park 904, 1098 XH, Amsterdam, Netherlands.
Notes
*Corresponding author. Email:
[email protected]
(A.D.);
[email protected]
(D.B.);
[email protected]
(S.W.)
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