Tuning microswimmer motility by liposome encapsulation: swimming and cargo transport of Chlamydomonas-encapsulating liposome

Abstract

Inspired by biology's use of vesicles for targeted transport, many studies have propelled liposomes with active matter, creating synthetic systems that can be viewed as microscale biohybrid robots. Nevertheless, the underlying motility mechanisms from a hydrodynamic perspective are often unresolved, and reliable velocity control remains challenging. Here we present a chlamylipo formed by encapsulating the motile alga Chlamydomonas reinhardtii within a giant liposome. We quantify how the characters of swimming change under controlled perturbations and, from a fluid-mechanical perspective, derive a deformation-velocity expression that incorporates liposome radius, beating frequency, and membrane protrusion. We further show that motility can be reversibly switched by incorporating light-responsive lipids, with the liposome acting as a "clutch" that modulates membrane-coupled propulsion. Thus, liposome encapsulation can function not only as a cargo compartment but also as a tunable motility regulator, enabling speed adjustment and reversible transitions between motile and non-motile states.

Figures (5)

• Figure 1: Typical swimming of chlamylipo.a Schematic illustration of the chlamylipo fabrication method. The water-in-oil emulsion-transfer method was employed to encapsulate the Chlamydomonas into the liposomes. b Long-term swimming behaviour of chlamylipo: the chlamylipo can actively swim even though the lipid membrane encloses the swimmer. The white scale bar represents 20 $\mathrm{\mu m}$. c Time-lapse sequence of a single swimming stroke. During the effective stroke, the Chlamydomonas pushes the liposome surface, causing the membrane protrusion; this non-reciprocal deformation allows the chlamylipo to propel itself. The black scale bar represents 5 $\mathrm{\mu m}$.
• Figure 2: Deformation-velocity relation of chlamylipo.a Schematic illustrating the variables extracted from image analysis. b Correlation matrix of the measured variables. c Deformation-velocity relation $p^*-U^*$ of chlamylipo. The experimental conditions were varied by changing the Chlamydomonas strains (wild-type CC-125 and oda1), or by changing the osmotic pressure of the outer solution relative to the inner solution (hypotonic, isotonic, and hypertonic). The inset reports the same $p^*-U^*$ data, with points color-coded by Chlamydomonas-to-liposome size ratio $\alpha_\mathrm{CL} = R_\mathrm{C}/R_\mathrm{L}$.
• Figure 3: Swimming characteristics under different experimental conditions. Comparisons of a the Chlamydomonas-to-liposome size ratio $\alpha_\mathrm{CL}$, b the swimming velocity $U$, c the dimensionless protrusion $p^*$, and d the beating frequency $f$. Boxes denote the first and third quartiles, with the red horizontal line showing the median; whiskers extend to 1.5$\times$ the inter-quartile range, and any data beyond this range are plotted individually. Statistical significance was evaluated with a two-sided Mann-Whitney U-test (*** $p < 0.001$, ** $p < 0.01$, * $p < 0.05$).
• Figure 4: Photoswitchable motility by utilizing membrane as a "clutch".a Schematic figure of the reversible motility photoswitching. The chlamylipo becomes motile with a UV pulse, while it can not swim after the blue light pulse. b Time history of the distance from the initial position $|\mathbf{x}(t) - \mathbf{x}(0)|$ and the swimming velocity $U$ from Supplemental Movie S4. Blue and purple vertical lines show the time of the blue light and UV pulses, respectively. c Time-lapsed snapshots from Supplemental Movie S4. The black scale bar represents 20 $\mathrm{\mu m}$. d Drawing letters "CL" by manipulating the chlamylipo trajectory with lights. The trajectory of the top figure is colored with the elapsed time, while the bottom figure is colored with the swimming velocity. The scatter-marker radius is inversely proportional to the velocity magnitude. The black scale bar represents 50 $\mathrm{\mu m}$.
• Figure 5: Cargo transport and release using chlamylipo.a Schematic figure of cargo transport using chlamylipo. b Snapshots of swimming chlamylipo containing micro-sized beads co-encapsulated with Chlamydomonas as cargo. Images are taken from Supplemental Movie S7. The black scale bar represents 10 $\mathrm{\mu m}$. c Cargo release from chlamylipo upon NIR laser irradiation. Co-encapsulated magnetic beads (i) were expelled as the liposome membrane burst (ii), followed by their diffusion away (iii). Images are taken from Supplemental Movie S8. The black scale bars represent 10 $\mathrm{\mu m}$.