Light-Powered Reactivation of Flagella and Contraction of Microtubule Networks: Toward Building an Artificial Cell

Abstract

Artificial systems capable of self-sustained movement with self-sufficient energy are of high interest with respect to the development of many challenging applications, including medical treatments, but also technical applications. The bottom-up assembly of such systems in the context of synthetic biology is still a challenging task. In this work, we demonstrate the biocompatibility and efficiency of an artificial light-driven energy module and a motility functional unit by integrating light-switchable photosynthetic vesicles with demembranated flagella. The flagellar propulsion is coupled to the beating frequency, and dynamic ATP synthesis in response to illumination allows us to control beating frequency of flagella in a light-dependent manner. In addition, we verified the functionality of light-powered synthetic vesicles in in vitro motility assays by encapsulating microtubules assembled with force-generating kinesin-1 motors and the energy module to investigate the dynamics of a contractile filamentous network in cell-like compartments by optical stimulation. Integration of this photosynthetic system with various biological building blocks such as cytoskeletal filaments and molecular motors may contribute to the bottom-up synthesis of artificial cells that are able to undergo motor-driven morphological deformations and exhibit directional motion in a light-controllable fashion.

Bio-hybrid micro-swimmers propelled by flagella isolated from C. reinhardtii†

“…2B). Beating frequency of axonemes depends on ATP concentration following a Michaelis-Menten-type kinetics [23, 37] with a linear trend at low amount of ATP and saturation at higher ATP concentrations around 1 mM. Following the addition of ATP, asymmetric bending waves initiate at the basal end (which is attached to a bead in Fig.…”

“…The possibility to externally modify flagellar wave components and beating frequency with light or chemical stimuli (such as calcium ions, as in Fig. 1B,D) 35,42–44 opens interesting perspective to control such a bio-hybrid micro-swimmer. The micro-swimmers, propelled by isolated and reactivated flagella, are potentially attractive to develop minimally invasive devices for medical applications, such as in vivo active cargo transport 7,8 .…”

Nano/Micromotors in Active Matter

“…Qu et al [94] proposed a similar method to control the flow field. Ahamd et al [95] synthesized light-driven energy vesicles containing bacteriorhodopsin, a light-driven proton pump that can actively transport proton across the cell membrane [96] and EF 0 F 1 -ATP synthase, which can use proton gradient to synthesize ATP. They adopted light-powered vesicles to control the beating frequency of flagella and the contraction of MT networks (Figure 8a).…”

Synthetic Cell as a Platform for Understanding Membrane-Membrane Interactions

“…The development of methods to create artificial photosynthetic entities expedited the translation of bacteriorhodopsin into applications in synthetic cells. Recently, artificial photosynthetic organelles were designed by Ahmad et al [113]. These nanometer-sized organelles were used to activate flagellar motion as well as contraction of microtubule networks by kinesin-1 motors.…”