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Motile behaviour of droplets in lipid systems

Abstract

Motility is the capacity for living organisms to move autonomously and with purpose, and is essential to life. The transition from abiotic chemistry into motile cellular compartments has yet to be understood, but motile behaviour likely followed chemical evolution because primeval cell survival depended on scouting for resources effectively. Minimalistic motile systems provide an experimental framework to delineate the emergence mechanisms of such an evolutionary asset. In this Review, we discuss frontier developments in controlling the movement of droplets in lipid systems, in particular, chemotactic behaviours driven by fluctuations in interfacial tension, because of its simple mechanism and prebiotic relevance. Although most efforts have focused on designing oil droplet motility in lipid-rich aqueous solutions, we highlight that water droplets can also move in lipid-enriched oils. First, we describe how droplets evolve chemotactic motility in lipid systems. Next, we review how these oil droplets can adapt their movement to illumination conditions. Finally, we discuss examples where chemical reactivity brings complexity to motility. This work contributes to systems chemistry, where chemical reactions combined with physicochemical phenomena can yield new functions, such that a limited set of molecules can promote complex movement at larger functional scales by following the rules of molecular chemistry.

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Fig. 1: Motile behaviour of droplets in a lipid-rich aqueous solution.
Fig. 2: Droplet motility from light-induced chemical reactions.
Fig. 3: Motile behaviour by coupling lipid systems with chemical reactions.
Fig. 4: Motility by formation of elastic filaments in water.
Fig. 5: Examples of speed dependence for motile droplets.

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Acknowledgements

N.K. thanks the European Research Council for funding (Consolidator Grant 772564). This work was supported by the Dutch Ministry of Education, Culture and Science (Gravity Program FMS 024.001.035). The authors thank the Animation Studio of the Institute for Complex Molecular Systems and Koen Pieterse (University of Eindhoven) for help with the illustrations.

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All authors researched data for the article, contributed substantially to discussion of the content and to the writing of the article. N.K. and D.B. finalized the article text. All authors reviewed and commented on the manuscript before submission.

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Correspondence to Nathalie Katsonis.

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Glossary

Protocells

Primitive, abiotic ‘original cells’. In chemistry, refers to chemical assemblies that display minimalistic functions or life-like characteristics, as seen in cells or microorganisms.

Lipids

Substances that are soluble in non-polar organic solvents and are usually insoluble in water. Lipids have possibly aided the emergence of life, because they form compartments in which catalytic networks can be formed. In this manuscript, we focus on lipids that contain a hydrophilic head and a hydrophobic tail.

Coacervate droplets

Membrane-free droplets formed through liquid–liquid phase separation.

Interfacial tension

Interfacial tension is the tendency of liquid interfaces at rest to shrink into the minimum surface area possible. Interfacial tension plays a key role when two non-miscible liquids are involved in a heterogeneous system.

Advecting

Transporting of molecules due to the bulk movement of liquid.

Reverse micelles

Micelles formed in oils with their hydrophilic head aligned inwards and hydrophobic tail outwards, encapsulating water inside the core.

Liquid crystals

Anisotropic molecules that exhibit a liquid crystalline phase in specific conditions of temperature (thermotropic liquid crystals) or dilution (lyotropic liquid crystals). The liquid crystal phase is characterized by fluidity as found in liquids, combined with long-range molecular orientation as found in crystals.

Nematic liquid crystal

A class of liquid crystals in which the molecules exhibit long-range order in molecular orientation but no positional order. The lack of periodic ordering makes them flow and, therefore, they can form droplets.

Topological defect

In liquid crystals, a topological defect is a point where the long-range ordering is absent or disrupted. The liquid crystalline order can be disrupted because of conflicting boundary conditions, in response to external stimuli or by phase transitions.

Isotropic transition temperature

Temperature of phase transition at which nematic liquid crystals transition into the isotropic state.

Cholesteric liquid crystal

A liquid crystal in which the molecules are organized into a helix, because a chiral component is present. Cholesteric liquid crystals are also known as chiral nematic liquid crystals.

Artificial molecular motors

Man-made molecules or molecular systems that perform useful tasks by converting energy into mechanically relevant motion.

Core–shell droplets

A microscopic compartment where one droplet is encapsulated inside another droplet dispersed in a liquid. The inner droplet is called the core and the droplet encapsulating it is called the shell.

Critical aggregation concentration

The concentration of lipids above which aggregates are formed. The aggregate types that form depends on the lipid structure.

Critical propulsion concentration

The minimum concentration of lipids that is required to initiate motility of droplets through solubilization by lipid aggregates. This concentration is larger than the critical aggregation concentration of lipids.

Belousov–Zhabotinsky (BZ) reaction

An oscillating chemical reaction where transition metal ions catalyse the oxidation of organic reductants in an acidic solution. The oscillatory cycles mediate the formation of complex chemical patterns in time and space.

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Babu, D., Katsonis, N., Lancia, F. et al. Motile behaviour of droplets in lipid systems. Nat Rev Chem 6, 377–388 (2022). https://doi.org/10.1038/s41570-022-00392-8

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