Bacteria as active colloids at fluid interfaces

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Degree type
Doctor of Philosophy (PhD)
Graduate group
Chemical and Biomolecular Engineering
Discipline
Engineering
Biochemistry, Biophysics, and Structural Biology
Subject
Active colloids
Bacteria
Hydrodynamics
Interface
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2022
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Author
Deng, Jiayi
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Abstract

The advent of active colloids that move absent external force brings important and as yet largely untapped degrees of freedom to interfacial engineering. The ability to design interfaces to incorporate self-propelled colloids as truly active surface elements relies on understanding how interfaces constrain swimming and modulate colloidal interactions. Bacteria and reactive Janus beads are examples of structures that propel themselves and interact with fluid boundaries. Bacteria also play essential roles in the global ecosystem, in industrial biotechnology, and in disease propagation. The ability to swim or self-propel allows motile bacteria to move through fluids to contact synthetic or natural boundaries, precipitating adhesion and colonization central to infection in vivo and the formation of deleterious biofilms in industrial settings. Hydrodynamic interactions and the chaotic nature of bacterial swimming give rise to intriguing non-equilibrium phenomena in active suspensions, including enhanced diffusion, long-range correlations in velocity and orientation fields and active phase separation. These findings have inspired biomimetic active colloid systems designed to recapitulate bacteria’s swimming and collective behavior. However, bacteria dynamics on fluid interfaces are not understood, despite the importance of interfaces in nature and the complexity of these highly anisotropic milieu. Interfaces between immiscible fluids are not only highly anisotropic domains in which viscosities change rapidly from one bulk fluid to the other, but are also high energy surfaces that promote colloid adsorption. Once adsorbed, colloidal scale objects typically become trapped with pinned contact lines where the two fluids intersect the particle. Furthermore, interfaces can have complex surface stresses including surface viscosities and Marangoni stresses owing to surfactant adsorption. These effects are associated with anomalous drag and divergence-free motion which further constrain the interfacial flow. While such factors have been shown to dramatically change the behaviors of passive colloids at interfaces and reconstructure its flow, their impact on the flow field generated by swimmers and their locomotion is unknown. In my thesis, I study the bacterium Pseudomonas aeruginosa PA01 as a model swimmer at aqueous- hexadecane interfaces. The bacteria can swim adjacent to the interface, or they can adsorb directly and swim in an adhered state with complex trajectories that differ from those in bulk in both form and spatio-temporal implications. In addition to characterizing the ensemble behavior of the bacteria, I have observed a gallery of distinct trajectories of individual swimmers on and near fluid interfaces. I find that most bacteria were trapped in the interfacial plane with fixed orientations of their bodies, indicating that the three-phase contact lines were pinned. These bacteria swim along curvilinear paths with trajectory radii of curvature that were correlated with the trapping configurations of their bodies. In addition to thermal diffusion, active noise attributed to switching between pusher and puller modes, instabilities of the flagellum, and interactions with other bacteria lead to active diffusion of the swimmer’s centers of rotation which randomized the bacterium’s displacement over long lag times. To understand their impact on interfacial transport, I visualize the interfacial flows generated by PA01 in pusher modes and find flow fields with unexpected symmetries that differ significantly from their bulk fluid counterparts. Analysis reveals that these flow fields can be decomposed into two dipolar hydrodynamic modes associated with incompressible interfaces. The relative importance of these modes is determined by the cell bodies’ trapped configurations. Hydrodynamic theory allows fundamental understanding of this flow field and its implications on mixing in the interface. I find that bacteria swimming alters factors essential to bacteria survival. These include interactions with passive structures and neighboring swimmers resulting in complex scattering that promotes mixing. P. aeruginosa are monotrichous bacteria that move as either pushers or pullers depending on the rotational sense of their single flagellum. For interfacially trapped bacteria, I discover the swimming paths for run and reverse modes differ significantly. Our hydrodynamic analysis suggests that the asymmetric swimming behavior is regulated by the re-orientation of the bacterial flagellum due to the buckling of hook. The interfacial flow around puller bacterium reveals the diverse forces and torques distributed around the bacterium due to its detailed body alignment. By understanding the motion and hydrodynamics of biological swimmers at fluid interfaces, we can develop design rules for artificial biomimetic systems to promote transport at fluid interfaces with broad implications in chemical engineering processes.

Advisor
Stebe, Kathleen, J
Date of degree
2022
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