Chemotaxis to self-generated AI-2 promotes biofilm formation in Escherichia coli

Jani, Sneha; Seely, Andrew L.; Peabody, George L.; Jayaraman, Arul; Manson, Michael D.

doi:10.1099/mic.0.000567

Cited by 44 publications

(64 citation statements)

References 58 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…It allows bacteria to navigate in environmental gradients of various chemicals [ 25 – 27 ] in order to locate conditions that are beneficial for growth [ 28 ]. Chemotaxis to self-secreted signals can also mediate collective behaviors, such as the autoinducer-2 dependent autoaggregation and biofilm formation by E. coli [ 29 , 30 ]. The chemotactic signal transduction pathway of E. coli includes two high-abundance (or major) receptors, Tsr and Tar, as well as three low-abundance (or minor) receptors, Trg, Tap, and Aer.…”

Section: Introductionmentioning

confidence: 99%

Chemotaxis of Escherichia coli to major hormones and polyamines present in human gut

Lopes

Sourjik

2018

The ISME Journal

View full text Add to dashboard Cite

The microorganisms in the gastrointestinal (GI) tract can influence the metabolism, immunity, and behavior of animal hosts. Increasing evidence suggests that communication between the host and the microbiome also occurs in the opposite direction, with hormones and other host-secreted compounds being sensed by microorganisms. Here, we addressed one key aspect of the host–microbe communication by studying chemotaxis of a model commensal bacterium, Escherichia coli, to several compounds present abundantly in the GI tract, namely catecholamines, thyroid hormones, and polyamines. Our results show that E. coli reacts to five out of ten analyzed chemicals, sensing melatonin, and spermidine as chemorepellents and showing mixed responses to dopamine, norepinephrine and 3,4-dihydroxymandelic acid. The strongest repellent response was observed for the polyamine spermidine, and we demonstrate that this response involves the low-abundance chemoreceptor Trg and the periplasmic binding protein PotD of the spermidine uptake system. The chemotactic effects of the tested compounds apparently correlate with their influence on growth and their stability in the GI tract, pointing to the specificity of the observed behavior. We hypothesize that the repellent responses observed at high concentrations of chemoeffective compounds might enable bacteria to avoid harmful levels of hormones and polyamines in the gut and, more generally, antimicrobial activities of the mucous layer.

show abstract

Section: Introductionmentioning

confidence: 99%

Chemotaxis of Escherichia coli to major hormones and polyamines present in human gut

Lopes

Sourjik

2018

The ISME Journal

View full text Add to dashboard Cite

show abstract

“…AI-2 is the only known QS molecule produced by the enteric bacterium Escherichia coli , and its production and uptake were shown to affect several E. coli phenotypes, including biofilm formation, motility, and virulence ( 21 , 22 ). Previous work showed that, during autoaggregation or biofilm formation by E. coli , AI-2 serves as a chemoattractant that recruits planktonic cells to growing cell aggregates ( 23 – 25 ). However, it remained unclear whether and how E. coli could use this AI-2-mediated autoaggregation in mixed microbial communities in which it represents only a minor fraction of the population.…”

Section: Introductionmentioning

confidence: 99%

Autoinducer 2-Dependent Escherichia coli Biofilm Formation Is Enhanced in a Dual-Species Coculture

Laganenka

Sourjik

2018

Appl Environ Microbiol

View full text Add to dashboard Cite

Biofilms in nature typically consist of multiple species, and microbial interactions are likely to have crucial effects on biofilm development, structure, and functions. The best-understood form of communication within bacterial communities involves the production, release, and detection of signal molecules (autoinducers), known as quorum sensing. Although autoinducers mainly promote intraspecies communication, autoinducer 2 (AI-2) is produced and detected by a variety of bacteria, thus principally allowing interspecies communication. Here we show the importance of AI-2-mediated signaling in the formation of mixed biofilms by Enterococcus faecalis and Escherichia coli. Our results demonstrate that AI-2 produced by E. faecalis promotes collective behaviors of E. coli at lower cell densities, enhancing autoaggregation of E. coli but also leading to chemotaxis-dependent coaggregation between the two species. Finally, we show that formation of such mixed dual-species biofilms increases the stress resistance of both E. coli and E. faecalis.IMPORTANCE The role of interspecies communication in the development of mixed microbial communities is becoming increasingly apparent, but specific examples of such communication remain limited. The universal signal molecule AI-2 is well known to regulate cell-density-dependent phenotypes of many bacterial species but, despite its potential for interspecies communication, the role of AI-2 in the establishment of multispecies communities is not well understood. In this study, we explore AI-2 signaling in a dual-species community containing two bacterial species that naturally cooccur in their mammalian hosts, i.e., Escherichia coli and Enterococcus faecalis. We show that active production of AI-2 by E. faecalis allows E. coli to perform collective behaviors at low cell densities. Additionally, AI-2- and chemotaxis-dependent coaggregation with E. faecalis creates nucleation zones for rapid growth of E. coli microcolonies in mixed biofilms and enhances the stress resistance of both species.

show abstract

“…The escape band is a general phenomenon not limited by specific chemoattractants or receptors, and it should be physiologically relevant, as it enhances the fitness of the population by avoiding being trapped by nonmetabolizable or weakly metabolizable attractants, such as AI-2 in the biofilm (32,33) and DHMA for commensal bacteria in the gut microbiota (34,35). Indeed, our model showed that the overall population growth starving E.coli growing E.coli rate increases as the system changes from the no-band-forming regime to the band-forming regime (SI Appendix, Fig.…”

Section: Summary and Discussionmentioning

confidence: 99%

Escape band in Escherichia coli chemotaxis in opposing attractant and nutrient gradients

Zhang

Dong

et al. 2019

Proc. Natl. Acad. Sci. U.S.A.

View full text Add to dashboard Cite

It is commonly believed that bacterial chemotaxis helps cells find food. However, not all attractants are nutrients, and not all nutrients are strong attractants. Here, by using microfluidic experiments, we studiedEscherichia colichemotaxis behavior in the presence of a strong chemoattractant (e.g., aspartate or methylaspartate) gradient and an opposing gradient of diluted tryptone broth (TB) growth medium. Our experiments showed that cells initially accumulate near the strong attractant source. However, after the peak cell density (h) reaches a critical valuehc, the cells form a “escape band” (EB) that moves toward the chemotactically weaker but metabolically richer nutrient source. By using various mutant strains and varying experimental conditions, we showed that the competition between Tap and Tar receptors is the key molecular mechanism underlying the formation of the escape band. A mathematical model combining chemotaxis signaling and cell growth was developed to explain the experiments quantitatively. The model also predicted that the width w and the peak positionxpof EB satisfy two scaling relations:w/l∼(h/hc)−1/2and1−xp/l∼(h/hc)−1/2, where l is the channel length. Both scaling relations were verified by experiments. Our study shows that the combination of nutrient consumption, population growth, and chemotaxis with multiple receptors allows cells to search for optimal growth condition in complex environments with conflicting sources.

show abstract

Chemotaxis to self-generated AI-2 promotes biofilm formation in Escherichia coli

Cited by 44 publications

References 58 publications

Chemotaxis of Escherichia coli to major hormones and polyamines present in human gut

Chemotaxis of Escherichia coli to major hormones and polyamines present in human gut

Autoinducer 2-Dependent Escherichia coli Biofilm Formation Is Enhanced in a Dual-Species Coculture

Escape band in Escherichia coli chemotaxis in opposing attractant and nutrient gradients

Contact Info

Product

Resources

About