Swimming Despite Obstacles: Bacterial Swimming as an Evolution-selected Feature
2022-08
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Swimming Despite Obstacles: Bacterial Swimming as an Evolution-selected Feature
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2022-08
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Abstract
In the 1670s, Leeuwenhoek used a single-lens microscope to bring the unfamiliar microscopic world of bacteria to human attention. In this research work, we use biophysical tools of quantitative microscopy and fluid dynamics to revisit the same world of microbes and shed light on the intricate yet fascinating motion of microbes. In particular, this thesis details two fundamentally significant problems related to microbial locomotion: 1) motility of microbes in complex fluids, and 2) impact of multiflagellarity on bacterial motility. Locomotion of flagellated microorganisms is of great importance for a wide range of biological processes from disease infection, to reproduction, and to ecosystem health. Bacterial swimming in simple Newtonian fluids is well understood; however, our understanding of their motion in their natural habitats comprising of microscopic particles and polymers is still far from complete. Even after six decades of research, whether bacteria show motility enhancement in polymer solutions and what is the origin of this enhancement remain under debate. We tackled this problem from a new perspective: we studied bacterial locomotion in dilute colloidal suspensions, which do not exhibit complex rheological behaviors such as shear thinning, thickening, etc. Surprisingly, we found that all the measurable swimming features of bacteria in colloidal suspensions are quantitatively the same as those in polymer solutions. This suggests a common origin of bacterial motility enhancement in all complex fluids and challenges all the existing theories which exclusively used polymer dynamics to explain this behavior. We subsequently developed a simple hydrodynamic model considering the colloidal nature of complex fluids, which predicted bacterial motility enhancement in both colloidal suspensions and polymer solutions. We also propose a new mechanism of bacterial wobbling that shows the enhancement and also reproduced bacterial helical trajectories with large pitches—another puzzling behavior of bacterial locomotion. Thus, our study combining experiments and theory unambiguously resolved the long-standing controversy of two problems at once, i.e., the origin of bacterial motility enhancement in complex fluids and the mechanism of bacterial wobbling in Newtonian fluids. Bacterial species also show variations in their flagellar architecture and adapt two common arrangements: monotrichous or uniflagellar bacteria possess a single flagellum at the pole of their body and peritrichous bacteria grow multiple flagella over their body, which form a helical rotating bundle propelling bacterial swimming. Although the cellular features of bacteria are under strong evolutionary selective pressures, extensive studies suggest that multiflagellarity confers no noticeable benefit to bacterial motility. These findings pose a long-standing question: why does multiflagellarity emerge in bacteria given the tremendous metabolic cost of flagellar synthesis? Here, contrary to common views that seek the answer beyond the basic function of flagella in motility, we show that multiflagellarity indeed provides a significant selective advantage in bacterial motility, allowing bacteria to maintain a constant swimming speed over a wide range of body sizes. Through experiments of immense sample sizes and detailed hydrodynamic modeling and simulations, we quantitatively reveal how bacteria utilize the increasing number of flagella to regulate the flagellar motor load, which leads to faster flagellar rotational speeds balancing the higher hydrodynamic drag on the bacterial body of larger sizes. Without such an elegant mechanism, the swimming speeds of uniflagellar bacteria decrease with increasing body sizes. This stark difference between the two swimming modes provides a novel fluid dynamic insight into the crucial role of multiflagellarity in maintaining optimum motility for navigation and survival in their native habitats.
Beyond, the ecological implications, results, and insights from this thesis serve as guidelines for devising artificial swimmers that efficiently navigate complex biological environments for drug delivery.
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University of Minnesota Ph.D. dissertation. August 2022. Major: Chemical Engineering. Advisors: Xiang Cheng, lorraine Francis. 1 computer file (PDF); xxiii, 120 pages.
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Kamdar, Shashank. (2022). Swimming Despite Obstacles: Bacterial Swimming as an Evolution-selected Feature. Retrieved from the University Digital Conservancy, https://hdl.handle.net/11299/259738.
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