Active cellular flows: biological networks, cytoplasmic streaming and swimming bacteria

Fluid flows play fundamental roles in biology, governing processes such as locomotion and transport. At the intraorganellar and intracellular scale, flows enable effective transport and mixing in systems where diffusion is insufficient to sustain the cell's metabolic and developmental needs. Fluid flows created by cellular appendages also govern how microorganisms self-propel in various settings. This thesis examines a diverse range of biological problems in which microscale fluid dynamics takes on a central role, spanning the organellar to the cell population scales. In the first half of the thesis, we study intracellular flows, beginning with flows inside the Endoplasmic Reticulum (ER), a network of tubules and membranous sheets inside a cell. Timely transport of ER contents is essential to its biological function, but its biophysical origin remains unknown. It has been recently proposed that this transport may be enabled by active contractions of ER tubules. To surmount the experimental challenges posed by a nanofluidic ER, we construct a viscous hydraulic model emulating flows and transport inside actively contracting networks. Our results indicate that biologically realistic tubule contractions cannot reproduce the experimentally measured tracer speeds, while contractions of perinuclear sheets generate local flows with only a short-range effect on luminal transport. Only contractions of peripheral sheets can reproduce experimental measurements, provided they contract fast enough. We next study flows on a cell-wide scale, in the Drosophila melanogaster embryo, a classical model system for eukaryotic development. It is a large, elongated cell containing numerous nuclei that must spread uniformly within the shared cytoplasm to ensure proper development. This spreading is facilitated by cytoplasmic flows driven by the cortex, a contractile cytoskeletal layer at the cell boundary. Modelling the problem as boundary-driven Stokes flows in a spheroidal cell, we first present an exact spheroidal harmonics solution. Applying our results to experiments, we show that the biological cortical flows are finely tuned to achieve near-optimal nuclear spreading. Lubrication theory produces an even simpler solution, applicable to more general cell geometries and incurring errors below 5% compared with the exact solution. An application of this lubrication result to transport leads to fully analytical solutions for the nuclear concentration that capture the essential physics of the system, including optimal axial spreading of nuclei. We further extend our lubrication solution to cytoplasmic flows in other biological cells driven by active forces at the cell boundary, including the forcing from cargo transport along actin filaments in plant cells. Specifically, we apply our lubrication methods to predict flows and stresses in four systems of biological significance: the Drosophila and C. elegans embryos (including pseudocleavage furrow formation), the pollen tube of seed plants, and plant root hair cells. Our results showcase the elegance and accuracy of asymptotic solutions in capturing the complex flows and stress patterns in diverse biological contexts, reinforcing its utility as a robust tool for cellular biophysics. The latter half of the thesis concerns fluid flows outside cells and focuses on bacterial locomotion. We begin by examining the fluid dynamics of rotating helical filaments, an archetypal low-Re propulsion strategy. In a classical 1976 paper, Lighthill calculated the ‘optimal’ resistance coefficients in a local resistive-force theory that best approximates predictions from the nonlocal slender-body theory for force-free swimming of a rotating helix without an attached load. These coefficients have since been widely used, often beyond the conditions under which they were derived. Here, we revisit the problem in the presence of a load, such as a bacterial cell body. We show that the optimal resistance coefficients depend in fact on the size of the load, and we quantify the increasing inaccuracy of Lighthill’s coefficients as the load grows. Finally, we provide a physical explanation for the origin of this unexpected load-dependence. We next investigate an aspect of bacterial locomotion near a wall. Flagellated bacteria are hydrodynamically attracted to rigid walls, but past work shows a `hovering' state where they swim stably at a finite height above surfaces. We use numerics and theory to reveal the physical origin of hovering. Simulations first show that hovering requires an elongated cell body and results from a tilt away from the wall. Theoretical models then identify two essential asymmetries: the response of width-asymmetric cells to active flows created by length-asymmetric cells. A minimal model reconciles near and far-field hydrodynamics, capturing all key features of hovering. Finally, we study fluid dynamics on the scale of cell populations, focusing on bacterial vortices in a cylinder. E. coli bacteria are known to swim in CCW circles above rigid surfaces, but in a cylindrical microwell with top-bottom asymmetric boundary conditions, they segregate into two populations of different sizes at opposite flat boundaries, and the smaller population reverses rotational direction. This motivates a flow singularities model for the motion of a population of chiral swimmers near one flat boundary of a cylindrical geometry subject to the flows created by a bacterial vortex at the opposite surface. We show that, purely based on hydrodynamic interactions, a bacterial vortex reverses rotational direction in the presence of a sufficiently large bacterial vortex at the opposite surface. Through the several distinct problems explored in this thesis, we thus illustrate the importance of fluid flows in biology, and highlight fluid dynamics as a valuable tool for understanding a range of biological and biophysical phenomena, inside and outside the cell.

Name dc:type.qualificationname

Doctor of Philosophy (PhD)

Level dc:type.qualificationlevel

Doctoral

Grantor dc:publisher.institution

University of Cambridge

Year dc:date.issued

2025

Author dc:creator

• Htet, Pyae Hein

Advisor dc:contributor.advisor

• Lauga, Eric

• biophysics
• cytoplasmic streaming
• fluid dynamics
• microswimmers

Licence

• https://apollo8-f-pro.lib.cam.ac.uk/bitstreams/caed78a9-b625-45d5-b6bc-f4244dcafebb/download
• http://purl.org/NET/rdflicense/allrightsreserved

Author Identifier

0000-0001-5068-9828

OAI identifier oai:identifier

oai:www.repository.cam.ac.uk:1810/386723