Chemotaxis and autoinducer-2 signalling mediate colonization and contribute to co-existence of Escherichia coli strains in the murine gut

Laganenka, Leanid; Lee, Jae Woo; Malfertheiner, Lukas; Dieterich, Cora; Fuchs, Lea; Piel, Jörn; Mering, Christian von; Sourjik, Victor; Hardt, Wolf‐Dietrich

doi:10.1038/s41564-022-01286-7

Cited by 17 publications

(13 citation statements)

References 86 publications

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“…However, even in these strains, expression levels remain bounded by the critical level at which swimming velocity saturates, indicating that cells avoid unnecessary resource expenditures that provide no additional bene t. Expression levels in other E. coli isolates map to different points on the expression-swimming curve, covering the range below saturation of motility. Such heterogeneity could be due to different selection pressures on motility in the ecological niches occupied by these isolates, which is consistent with ndings that differences in motility allow coexistence and niche segregation between E. coli strains, both in vitro 25 and in an animal host 47 .…”

Section: Discussionsupporting

confidence: 88%

Physics and physiology determine strategies of bacterial investment in flagellar motility

Sourjik,

Lisevich,

Colin

et al. 2024

Preprint

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Regulatory strategies that allow microorganisms to balance their investment of limited resources in different physiological functions remain poorly understood, particularly for numerous cellular functions that are not directly required for growth. Here, we investigate the allocation of resources to flagellar swimming, the most prominent and costly behavior in bacteria that is not directly required for growth. We show that the dependence of motile behavior on gene expression is determined by the hydrodynamics of propulsion, which limits the ability of bacteria to increase their swimming by synthesizing more than a critical number of flagellar filaments. Together with the fitness cost of flagellar biosynthesis, this defines the physiologically relevant range of investment in motility. Gene expression in all E. coli isolates tested falls within this range, with many strains maximizing motility under nutrient-rich conditions, particularly when grown on a porous medium. The hydrodynamics of swimming may further explain the bet-hedging behavior observed at low levels of motility gene expression.

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Section: Discussionsupporting

confidence: 88%

Physics and physiology determine strategies of bacterial investment in flagellar motility

Sourjik,

Lisevich,

Colin

et al. 2024

Preprint

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“…Expression levels in other E. coli isolates map to different points on the expression-swimming curve, covering the range below saturation of motility. Such heterogeneity could be due to different selection pressures on motility in the ecological niches occupied by these isolates, which is consistent with findings that differences in motility allow coexistence and niche segregation between E. coli strains, both in vitro 25 and in an animal host 47 .…”

Section: Discussionsupporting

confidence: 88%

Physics and physiology determine strategies of bacterial investment in flagellar motility

Lisevich,

Colin,

Yang

et al. 2024

Preprint

Self Cite

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Regulatory strategies that allow microorganisms to balance their investment of limited resources in different physiological functions remain poorly understood, particularly for numerous cellular functions that are not directly required for growth. Here, we investigate the allocation of resources to flagellar swimming, the most prominent and costly behavior in bacteria that is not directly required for growth. We show that the dependence of motile behavior on gene expression in Escherichia coli is determined by the hydrodynamics of propulsion, which limits the ability of bacteria to increase their swimming by synthesizing more than a critical number of flagellar filaments. Together with the fitness cost of flagellar biosynthesis, this defines the physiologically relevant range of investment in motility. Gene expression in all E. coli isolates tested falls within this range, with many strains maximizing motility under nutrient-rich conditions, particularly when grown on a porous medium. The hydrodynamics of swimming may further explain the bet-hedging behavior observed at low levels of motility gene expression.

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“…This is an indication of an active role of AI-2 secretion and sensing in initiating ecological niche segregation [50,51], and therefore stable co-existence of different E. coli strains in spatially complex environments. This is supported by results of competitive experiments with E. coli in murine gut, where strains characterized by different AI-2 detection capability (WT and Δ lsrB ) coexist by occupying different niches [52].…”

Section: Discussionmentioning

confidence: 86%

“…We show that chemotaxis allows E. coli to colonize cavities such as the interspace between villi and crypts, where they likely outcompete local invaders due to their higher local population. Additionally, if a bacterial strain is able to detect AI-2 more efficiently than other strains, it may gain a competitive advantage, as shown by comparing a WT with a non-chemotactic mutant (Δ cheY ) [52]. Concentration and quality of carbon availability may also influence the bacterial chemotactic response.…”

Section: Discussionmentioning

confidence: 99%

Spatial structure, chemotaxis and quorum sensing shape biomass accumulation in complex systems

Scheidweiler

Bordoloi

Sentchilo

et al. 2023

Preprint

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Biological tissues, sediments, or engineered systems are spatially structured media with a tortuous and porous structure that host the flow of fluids. Such complex environments can influence the spatial and temporal colonization patterns of bacteria by controlling the transport of individual bacterial cells, the availability of resources, and the distribution of chemical signals for communication. Yet, due to the multi-scale structure of these complex systems, it is hard to assess how different biotic and abiotic properties work together to control the accumulation of bacterial biomass. Here, we explore how flow mediated interactions allow the gut commensal Escherichia coli to colonize a porous structure that is composed of heterogenous dead-end pores (DEPs) and connecting percolating channels, i.e. transmitting pores (TPs), mimicking the structured surface of mammalian guts. We find that in presence of flow, gradients of the quorum sensing (QS) signaling molecule autoinducer-2 (AI-2) promote E. coli chemotactic accumulation in the DEPs. In this crowded environment, the combination of growth and cell-to-cell collision favors the development of suspended bacterial aggregates. This results in hot-spots of resource consumption, which, upon resource limitation, triggers the mechanical evasion of biomass from glucose and oxygen depleted DEPs. Our findings demonstrate that microscale medium structure and complex flow coupled with bacterial quorum sensing and chemotaxis control the heterogenous accumulation of bacterial biomass in a spatially structured environment, such as villi and crypts in the gut or in tortuous pores within soil and filters.

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Chemotaxis and autoinducer-2 signalling mediate colonization and contribute to co-existence of Escherichia coli strains in the murine gut

Cited by 17 publications

References 86 publications

Physics and physiology determine strategies of bacterial investment in flagellar motility

Physics and physiology determine strategies of bacterial investment in flagellar motility

Physics and physiology determine strategies of bacterial investment in flagellar motility

Spatial structure, chemotaxis and quorum sensing shape biomass accumulation in complex systems

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