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Decoding the hydrodynamic properties of microscale helical propellers from Brownian fluctuations
The complex motility of bacteria, ranging from single-swimmer behaviors such as chemotaxis to collective dynamics, including biofilm formation and active matter phenomena, is driven by their microscale propellers. Despite extensive study of swimming flagellated bacteria, the hydrodynamic properties...
Autores principales: | , , , , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
National Academy of Sciences
2023
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10235983/ https://www.ncbi.nlm.nih.gov/pubmed/37235635 http://dx.doi.org/10.1073/pnas.2220033120 |
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author | Djutanta, Franky Brown, Peter T. Nainggolan, Bonfilio Coullomb, Alexis Radhakrishnan, Sritharini Sentosa, Jason Yurke, Bernard Hariadi, Rizal F. Shepherd, Douglas P. |
author_facet | Djutanta, Franky Brown, Peter T. Nainggolan, Bonfilio Coullomb, Alexis Radhakrishnan, Sritharini Sentosa, Jason Yurke, Bernard Hariadi, Rizal F. Shepherd, Douglas P. |
author_sort | Djutanta, Franky |
collection | PubMed |
description | The complex motility of bacteria, ranging from single-swimmer behaviors such as chemotaxis to collective dynamics, including biofilm formation and active matter phenomena, is driven by their microscale propellers. Despite extensive study of swimming flagellated bacteria, the hydrodynamic properties of their helical-shaped propellers have never been directly measured. The primary challenges to directly studying microscale propellers are 1) their small size and fast, correlated motion, 2) the necessity of controlling fluid flow at the microscale, and 3) isolating the influence of a single propeller from a propeller bundle. To solve the outstanding problem of characterizing the hydrodynamic properties of these propellers, we adopt a dual statistical viewpoint that connects to the hydrodynamics through the fluctuation–dissipation theorem (FDT). We regard the propellers as colloidal particles and characterize their Brownian fluctuations, described by 21 diffusion coefficients for translation, rotation, and correlated translation–rotation in a static fluid. To perform this measurement, we applied recent advances in high-resolution oblique plane microscopy to generate high-speed volumetric movies of fluorophore-labeled, freely diffusing Escherichia coli flagella. Analyzing these movies with a bespoke helical single-particle tracking algorithm, we extracted trajectories, calculated the full set of diffusion coefficients, and inferred the average propulsion matrix using a generalized Einstein relation. Our results provide a direct measurement of a microhelix’s propulsion matrix and validate proposals that the flagella are highly inefficient propellers, with a maximum propulsion efficiency of less than 3%. Our approach opens broad avenues for studying the motility of particles in complex environments where direct hydrodynamic approaches are not feasible. |
format | Online Article Text |
id | pubmed-10235983 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2023 |
publisher | National Academy of Sciences |
record_format | MEDLINE/PubMed |
spelling | pubmed-102359832023-11-26 Decoding the hydrodynamic properties of microscale helical propellers from Brownian fluctuations Djutanta, Franky Brown, Peter T. Nainggolan, Bonfilio Coullomb, Alexis Radhakrishnan, Sritharini Sentosa, Jason Yurke, Bernard Hariadi, Rizal F. Shepherd, Douglas P. Proc Natl Acad Sci U S A Physical Sciences The complex motility of bacteria, ranging from single-swimmer behaviors such as chemotaxis to collective dynamics, including biofilm formation and active matter phenomena, is driven by their microscale propellers. Despite extensive study of swimming flagellated bacteria, the hydrodynamic properties of their helical-shaped propellers have never been directly measured. The primary challenges to directly studying microscale propellers are 1) their small size and fast, correlated motion, 2) the necessity of controlling fluid flow at the microscale, and 3) isolating the influence of a single propeller from a propeller bundle. To solve the outstanding problem of characterizing the hydrodynamic properties of these propellers, we adopt a dual statistical viewpoint that connects to the hydrodynamics through the fluctuation–dissipation theorem (FDT). We regard the propellers as colloidal particles and characterize their Brownian fluctuations, described by 21 diffusion coefficients for translation, rotation, and correlated translation–rotation in a static fluid. To perform this measurement, we applied recent advances in high-resolution oblique plane microscopy to generate high-speed volumetric movies of fluorophore-labeled, freely diffusing Escherichia coli flagella. Analyzing these movies with a bespoke helical single-particle tracking algorithm, we extracted trajectories, calculated the full set of diffusion coefficients, and inferred the average propulsion matrix using a generalized Einstein relation. Our results provide a direct measurement of a microhelix’s propulsion matrix and validate proposals that the flagella are highly inefficient propellers, with a maximum propulsion efficiency of less than 3%. Our approach opens broad avenues for studying the motility of particles in complex environments where direct hydrodynamic approaches are not feasible. National Academy of Sciences 2023-05-26 2023-05-30 /pmc/articles/PMC10235983/ /pubmed/37235635 http://dx.doi.org/10.1073/pnas.2220033120 Text en Copyright © 2023 the Author(s). Published by PNAS. https://creativecommons.org/licenses/by-nc-nd/4.0/This article is distributed under Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND) (https://creativecommons.org/licenses/by-nc-nd/4.0/) . |
spellingShingle | Physical Sciences Djutanta, Franky Brown, Peter T. Nainggolan, Bonfilio Coullomb, Alexis Radhakrishnan, Sritharini Sentosa, Jason Yurke, Bernard Hariadi, Rizal F. Shepherd, Douglas P. Decoding the hydrodynamic properties of microscale helical propellers from Brownian fluctuations |
title | Decoding the hydrodynamic properties of microscale helical propellers from Brownian fluctuations |
title_full | Decoding the hydrodynamic properties of microscale helical propellers from Brownian fluctuations |
title_fullStr | Decoding the hydrodynamic properties of microscale helical propellers from Brownian fluctuations |
title_full_unstemmed | Decoding the hydrodynamic properties of microscale helical propellers from Brownian fluctuations |
title_short | Decoding the hydrodynamic properties of microscale helical propellers from Brownian fluctuations |
title_sort | decoding the hydrodynamic properties of microscale helical propellers from brownian fluctuations |
topic | Physical Sciences |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10235983/ https://www.ncbi.nlm.nih.gov/pubmed/37235635 http://dx.doi.org/10.1073/pnas.2220033120 |
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