Physics of swimming and its fitness cost determine strategies of bacterial investment in flagellar motility

Abstract Microorganisms must distribute their limited resources among different physiological functions, including those that do not directly contribute to growth. In this study, we investigate the allocation of resources to flagellar swimming, the most prominent and biosynthetically costly of such...

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Main Authors: Irina Lisevich, Remy Colin, Hao Yuan Yang, Bin Ni, Victor Sourjik
Format: Article
Language:English
Published: Nature Portfolio 2025-02-01
Series:Nature Communications
Online Access:https://doi.org/10.1038/s41467-025-56980-x
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author Irina Lisevich
Remy Colin
Hao Yuan Yang
Bin Ni
Victor Sourjik
author_facet Irina Lisevich
Remy Colin
Hao Yuan Yang
Bin Ni
Victor Sourjik
author_sort Irina Lisevich
collection DOAJ
description Abstract Microorganisms must distribute their limited resources among different physiological functions, including those that do not directly contribute to growth. In this study, we investigate the allocation of resources to flagellar swimming, the most prominent and biosynthetically costly of such cellular functions in bacteria. Although the growth-dependence of flagellar gene expression in peritrichously flagellated Escherichia coli is well known, the underlying physiological limitations and regulatory strategies are not fully understood. By characterizing the dependence of motile behavior on the activity of the flagellar regulon, we demonstrate that, beyond a critical number of filaments, the hydrodynamics of propulsion limits the ability of bacteria to increase their swimming by synthesizing additional flagella. In nutrient-rich conditions, E. coli apparently maximizes its motility until reaching this limit, while avoiding the excessive cost of flagella production. Conversely, during carbon-limited growth motility remains below maximal levels and inversely correlates with the growth rate. The physics of swimming may further explain the selection for bimodal resource allocation in motility at low average expression levels. Notwithstanding strain-specific variation, the expression of flagellar genes in all tested natural isolates of E. coli also falls within the same range defined by the physical limitations on swimming and its biosynthetic cost.
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spelling doaj-art-2d48424a97f6441e8d8c8d81352712292025-08-20T02:15:11ZengNature PortfolioNature Communications2041-17232025-02-0116111310.1038/s41467-025-56980-xPhysics of swimming and its fitness cost determine strategies of bacterial investment in flagellar motilityIrina Lisevich0Remy Colin1Hao Yuan Yang2Bin Ni3Victor Sourjik4Max Planck Institute for Terrestrial Microbiology & Center for Synthetic Microbiology (SYNMIKRO), Karl-von-Frisch-Strasse 14Max Planck Institute for Terrestrial Microbiology & Center for Synthetic Microbiology (SYNMIKRO), Karl-von-Frisch-Strasse 14Max Planck Institute for Terrestrial Microbiology & Center for Synthetic Microbiology (SYNMIKRO), Karl-von-Frisch-Strasse 14Max Planck Institute for Terrestrial Microbiology & Center for Synthetic Microbiology (SYNMIKRO), Karl-von-Frisch-Strasse 14Max Planck Institute for Terrestrial Microbiology & Center for Synthetic Microbiology (SYNMIKRO), Karl-von-Frisch-Strasse 14Abstract Microorganisms must distribute their limited resources among different physiological functions, including those that do not directly contribute to growth. In this study, we investigate the allocation of resources to flagellar swimming, the most prominent and biosynthetically costly of such cellular functions in bacteria. Although the growth-dependence of flagellar gene expression in peritrichously flagellated Escherichia coli is well known, the underlying physiological limitations and regulatory strategies are not fully understood. By characterizing the dependence of motile behavior on the activity of the flagellar regulon, we demonstrate that, beyond a critical number of filaments, the hydrodynamics of propulsion limits the ability of bacteria to increase their swimming by synthesizing additional flagella. In nutrient-rich conditions, E. coli apparently maximizes its motility until reaching this limit, while avoiding the excessive cost of flagella production. Conversely, during carbon-limited growth motility remains below maximal levels and inversely correlates with the growth rate. The physics of swimming may further explain the selection for bimodal resource allocation in motility at low average expression levels. Notwithstanding strain-specific variation, the expression of flagellar genes in all tested natural isolates of E. coli also falls within the same range defined by the physical limitations on swimming and its biosynthetic cost.https://doi.org/10.1038/s41467-025-56980-x
spellingShingle Irina Lisevich
Remy Colin
Hao Yuan Yang
Bin Ni
Victor Sourjik
Physics of swimming and its fitness cost determine strategies of bacterial investment in flagellar motility
Nature Communications
title Physics of swimming and its fitness cost determine strategies of bacterial investment in flagellar motility
title_full Physics of swimming and its fitness cost determine strategies of bacterial investment in flagellar motility
title_fullStr Physics of swimming and its fitness cost determine strategies of bacterial investment in flagellar motility
title_full_unstemmed Physics of swimming and its fitness cost determine strategies of bacterial investment in flagellar motility
title_short Physics of swimming and its fitness cost determine strategies of bacterial investment in flagellar motility
title_sort physics of swimming and its fitness cost determine strategies of bacterial investment in flagellar motility
url https://doi.org/10.1038/s41467-025-56980-x
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