Cell extract gels as an example of active matter

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Cell extract gels as an example of active matter Agnieszka Wisniewska1 · Tomasz Kalwarczyk1 · Jedrzej Szymanski2 · Katarzyna Kryszczuk1,3 · Kinga Matula1 · Robert Holyst1 Received: 24 September 2019 / Revised: 30 April 2020 / Accepted: 3 May 2020 / Published online: 21 June 2020 © The Author(s) 2020

Abstract Cell lysates (cellular extracts) constitute a perfect imitation of the intracellular environment that can provide insight into cellular response to external stimuli. However, most of the presented results are performed for diluted lysates that do not reflect the actual properties of a crowded cellular environment. Here, we report for the first time the measurement of the viscosity and shear storage modulus of highly concentrated Escherichia coli (E. coli) lysates with and without adenosine triphosphate (ATP). By cleavage of DNA content, we showed the value of shear storage modulus G decreases by 19–31% in comparison to control samples. The addition of molecules that provides energy (ATP) allowed to rebuild the structure of the lysate by reversibly increasing viscous properties over elastic ones. When the energy delivered in the form of ATP is consumed by the unliving bacterial lysate, the system returns to its initial state. Keywords Escherichia coli · E. coli · Lysate · Viscoelasticity · Adenosine triphosphate · ATP · Shear modulus

Introduction A concept of active matter—the ubiquitous nonequilibrium condensed system—has been developed for many years in the context of both living and nonliving matter (Marchetti et al. 2013; Palacci et al. 2010; Paxton et al. 2004; Parrish and Hamner 1997; Serra-Picamal et al. 2012). The active matter systems are composed of self-driven units, active particles, each capable of converting stored or ambient free energy into systematic movement (Schweitzer 2007). This energy-related concept is utilized in all biological systems on different scales, starting from cells (Kemkemer et al. 2000) or bacterial suspensions (Dombrowski et al. 2004) and with shoals of fish or flocks of birds (Ballerini et al. Electronic supplementary material The online version of this article (https://doi.org/10.1007/s00397-020-01213-9) contains supplementary material, which is available to authorized users.  Robert Holyst

[email protected] 1

Institute of Physical Chemistry, Polish Academy of Sciences, Kasprzaka 44/52, 01-224, Warsaw, Poland

2

Nencki Institute of Experimental Biology of the Polish Academy of Sciences, 3 Pasteur Street, 02-093, Warsaw, Poland

3

Faculty of Management, University of Warsaw, Szturmowa 1/3, 02-678, Warsaw, Poland

2008). In this paper, we present results on highly concentrated Escherichia coli (E. coli) lysate as an alternative system, in which the consumption and dissipation of energy in the form of added adenosine triphosphate (ATP) allow the system to changes its viscous and elastic properties. Foffano et al. (2012) simulated macroscopic shear experiments in active nematics and compared them with microrheology simulations where a spherical pr