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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...

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Autores principales: Djutanta, Franky, Brown, Peter T., Nainggolan, Bonfilio, Coullomb, Alexis, Radhakrishnan, Sritharini, Sentosa, Jason, Yurke, Bernard, Hariadi, Rizal F., Shepherd, Douglas P.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: National Academy of Sciences 2023
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.
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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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