Biphasic chemotaxis of
            <i>Escherichia coli</i>
            to the microbiota metabolite indole

Yang, Jingyun; Chawla, Ravi; Rhee, Kathy Y.; Gupta, Rachit; Manson, Michael D.; Jayaraman, Arul; Lele, Pushkar P.

doi:10.1073/pnas.1916974117

Cited by 50 publications

(58 citation statements)

References 65 publications

(80 reference statements)

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“…The response of the chemotaxis network to external stimuli is conventionally measured by determining the rotational bias ( Block et al, 1983 ; Yang et al, 2020 ; Lele et al, 2015 ; Jasuja et al, 1999 ). Tethering cells to glass surfaces is the preferred method of determining the rotational bias.…”

Section: Discussionmentioning

confidence: 99%

“…Increased CheY-P binding to the motor promotes CW rotation in an otherwise CCW rotating motor ( Sourjik and Wingreen, 2012 ). The output of the flagellar switch is quantified by the fraction of the time that the motor rotates CW, termed CW bias ( Block et al, 1983 ; Yuan et al, 2012 ; Yang et al, 2020 ). A decrease (increase) in CheY-P levels causes corresponding decrease (increase) in CW bias ( Cluzel et al, 2000 ; Scharf et al, 1998 ).…”

Section: Introductionmentioning

confidence: 99%

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Asymmetric random walks reveal that the chemotaxis network modulates flagellar rotational bias in Helicobacter pylori

Antani

Sumali

Lele

et al. 2021

eLife

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The canonical chemotaxis network modulates the bias for a particular direction of rotation in the bacterial flagellar motor to help the cell migrate toward favorable chemical environments. How the chemotaxis network in Helicobacter pylori modulates flagellar functions is unknown, which limits our understanding of chemotaxis in this species. Here, we determined that H. pylori swim faster (slower) whenever their flagella rotate counterclockwise (clockwise) by analyzing their hydrodynamic interactions with bounding surfaces. This asymmetry in swimming helped quantify the rotational bias. Upon exposure to a chemo-attractant, the bias decreased and the cells tended to swim exclusively in the faster mode. In the absence of a key chemotaxis protein, CheY, the bias was zero. The relationship between the reversal frequency and the rotational bias was unimodal. Thus, H. pylori’s chemotaxis network appears to modulate the probability of clockwise rotation in otherwise counterclockwise-rotating flagella, similar to the canonical network.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Asymmetric random walks reveal that the chemotaxis network modulates flagellar rotational bias in Helicobacter pylori

Antani

Sumali

Lele

et al. 2021

eLife

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“…Because indole-3-lactate can act as a ligand for AhR, we speculate that L. crispatus may regulate the IL-22-AhR response in the vagina, reducing the risk of vaginal candidiasis in the same way IAld does, and potentially activating the AhR response in newborns to prevent early-life candidiasis. Additionally, indole itself may play a role in structuring community composition by selecting for organisms that have adapted to a high abundance of this metabolite, repelling more transient microbes that have not been exposed to higher indole concentrations previously ( 39 ).…”

Section: Discussionmentioning

confidence: 99%

Cervicovaginal Microbiome Composition Is Associated with Metabolic Profiles in Healthy Pregnancy

Oliver

LaMere

Weihe

et al. 2020

mBio

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Microbes and their metabolic products influence early-life immune and microbiome development, yet remain understudied during pregnancy. Vaginal microbial communities are typically dominated by one or a few well-adapted microbes which are able to survive in a narrow pH range and are adapted to live on host-derived carbon sources, likely sourced from glycogen and mucin present in the vaginal environment. We characterized the cervicovaginal microbiomes of 16 healthy women throughout the three trimesters of pregnancy. Additionally, we analyzed saliva and urine metabolomes using gas chromatography-time of flight mass spectrometry (GC-TOF MS) and liquid chromatography-tandem mass spectrometry (LC-MS/MS) lipidomics approaches for samples from mothers and their infants through the first year of life. Amplicon sequencing revealed most women had either a simple community with one highly abundant species of Lactobacillus or a more diverse community characterized by a high abundance of Gardnerella, as has also been previously described in several independent cohorts. Integrating GC-TOF MS and lipidomics data with amplicon sequencing, we found metabolites that distinctly associate with particular communities. For example, cervicovaginal microbial communities dominated by Lactobacillus crispatus have high mannitol levels, which is unexpected given the characterization of L. crispatus as a homofermentative Lactobacillus species. It may be that fluctuations in which Lactobacillus dominate a particular vaginal microbiome are dictated by the availability of host sugars, such as fructose, which is the most likely substrate being converted to mannitol. Overall, using a multi-“omic” approach, we begin to address the genetic and molecular means by which a particular vaginal microbiome becomes vulnerable to large changes in composition. IMPORTANCE Humans have a unique vaginal microbiome compared to other mammals, characterized by low diversity and often dominated by Lactobacillus spp. Dramatic shifts in vaginal microbial communities sometimes contribute to the presence of a polymicrobial overgrowth condition called bacterial vaginosis (BV). However, many healthy women lacking BV symptoms have vaginal microbiomes dominated by microbes associated with BV, resulting in debate about the definition of a healthy vaginal microbiome. Despite substantial evidence that the reproductive health of a woman depends on the vaginal microbiota, future therapies that may improve reproductive health outcomes are stalled due to limited understanding surrounding the ecology of the vaginal microbiome. Here, we use sequencing and metabolomic techniques to show novel associations between vaginal microbes and metabolites during healthy pregnancy. We speculate these associations underlie microbiome dynamics and may contribute to a better understanding of transitions between alternative vaginal microbiome compositions.

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“…The unstuck cells were gently removed by wicking the fluid while adding buffer at the other end. The stuck cells were exposed to buffers of desired pH (5.0 to 9.0) containing 40 mM benzoate [33,36,51] for at least 5-10 min prior to the measurements.…”

Section: Modulation Of Intracellular Phmentioning

confidence: 99%

Protein expression-independent response of intensity-based pH-sensitive fluorophores in Escherichia coli

2020

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Fluorescent proteins that modulate their emission intensities when protonated serve as excellent probes of the cytosolic pH. Since the total fluorescence output fluctuates significantly due to variations in the fluorophore levels in cells, eliminating the dependence of the signal on protein concentration is crucial. This is typically accomplished with the aid of ratiometric fluorescent proteins such as pHluorin. However, pHluorin is excited by blue light, which can complicate pH measurements by adversely impacting bacterial physiology. Here, we characterized the response of intensity-based, pH-sensitive fluorescent proteins that excite at longer wavelengths where the blue light effect is diminished. The pH-response was interpreted in terms of an analytical model that assumed two emission states for each fluorophore: a low intensity protonated state and a high intensity deprotonated state. The model suggested a scaling to eliminate the dependence of the signal on the expression levels as well as on the illumination and photon-detection settings. Experiments successfully confirmed the scaling predictions. Thus, the internal pH can be readily determined with intensity-based fluorophores with appropriate calibrations irrespective of the fluorophore concentration and the signal acquisition setup. The framework developed in this work improves the robustness of intensity-based fluorophores for internal pH measurements in E. coli, potentially extending their applications.

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Biphasic chemotaxis of Escherichia coli to the microbiota metabolite indole

Cited by 50 publications

References 65 publications

Asymmetric random walks reveal that the chemotaxis network modulates flagellar rotational bias in Helicobacter pylori

Asymmetric random walks reveal that the chemotaxis network modulates flagellar rotational bias in Helicobacter pylori

Cervicovaginal Microbiome Composition Is Associated with Metabolic Profiles in Healthy Pregnancy

Protein expression-independent response of intensity-based pH-sensitive fluorophores in Escherichia coli

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