Interfacial deformations by active growth of oil-degrading bacteria on oil droplets

The study of active matter is crucial for unraveling the immense complexity of living systems. When confined to an interface, colonies of growing, rod-shaped cells form active nematic crystals, which exhibit long-range ordering and produce active stresses. While the properties of such monolayers on rigid surfaces are well understood, their behavior at deformable interfaces has not yet been described. Here, we show that the confined growth of non-motile, rod-shaped, bacteria on spherical oil droplets results in complex interfacial deformations. Using microfluidics, timelapse microscopy, and image analysis, buckling of the interface, tubulation, and bulk bio-aggregate formation are quantified on hundreds of droplets with 5 µm < R < 150 µm over 72 hours. Buckling is caused by jamming when cells form a monolayer at the interface, and is determined by the droplet radius and the rate of diffusive encounters between cells and droplets. The buckling instability has a characteristic wavelength that depends on the droplet radius, challenging existing models of the buckling of thin films. Tubular structures that extend from the interface are comparable in length to the initial droplet radius and are composed of an outer shell of bacteria that stabilize an inner filament of oil. These oil filaments break up into smaller microdroplets dispersed within the bacterial shell. Using a mechanistic model of tube extension, we show that interfacial deformations are caused by the exponential growth of cells in a monolayer. Comparison to other active nematics reveals remarkable similarities between the collective behaviors of systems in which the activity is due to (i) motility and (ii) growth. Interactions between oil-degrading bacteria and oil droplets are of great importance in the study of oil spill remediation. Bacterial biodegradation of immiscible oil is crucial for removing spilled oil from contaminated environments, and requires cell-droplet encounters, surface attachment, and hydrocarbon metabolism. Chemical dispersants are applied to oil spills to reduce the mean dispersed droplet size, thereby increasing the available surface area for attachment, in attempts to facilitate bacterial biodegradation. However, their effectiveness remains contentious as studies have shown that dispersants can inhibit or enhance biodegradation. Therefore, questions remain on whether dispersants affect surface attachment or cell viability. Using a custom microfluidic device, we decouple the effects of chemical dispersants on different biophysical parameters and show that dispersants do not inhibit attachment or growth of bacteria at the droplet surface. In conjunction with Monte Carlo simulations of buckling, it is shown that dispersant effectiveness for facilitating biodegradation depends on the cell concentration in the droplets’ vicinity. Finally, a hydrodynamic treadmill was built to obtain the first prolonged in vitro observations of rising oil droplets colonized and deformed by bacteria. Droplet deformations significantly decrease the rising speeds of droplets through the water column. Additionally, bio-aggregate formation can lead to oil sedimentation. These experiments allow us to describe how microscopic interactions contribute to macroscopic ecological processes. Our results could significantly improve current models of oil droplet transport.

Name thesis:degree_name

Ph.D.

Level thesis:degree_level

Dissertation

Discipline thesis:degree_discipline

Physics

Grantor

University of Illinois at Urbana-Champaign

Year dc:date

2022

Author dc:creator

• Hickl, Vincent

Contributors dc:contributor

• Juarez, Gabriel
• Golding, Ido
• Dahmen, Karin
• Gruebele, Martin

• Biophysics
• Soft Matter
• Experimental Physics
• Active Matter
• Active Nematics
• Microfluidics
• Microscopy
• Bacteria
• Biodegradation
• Oil Spill
• Fluid Mechanics
• Chemical Dispersants
• Oil Transport
• Droplets

Statement dc:rights

• Copyright 2022 Vincent Hickl

Language dc:language

en, eng

Handle dc:identifier

https://hdl.handle.net/2142/117771

OAI record oai:identifier

https://www.ideals.illinois.edu/oai-pmh?verb=GetRecord&metadataPrefix=etdms&identifier=oai%3Awww.ideals.illinois.edu%3A2142%2F117771