scholarly journals Chemotaxis towards autoinducer 2 mediates autoaggregation in Escherichia coli

2016 ◽  
Vol 7 (1) ◽  
Author(s):  
Leanid Laganenka ◽  
Remy Colin ◽  
Victor Sourjik

Abstract Bacteria communicate by producing and sensing extracellular signal molecules called autoinducers. Such intercellular signalling, known as quorum sensing, allows bacteria to coordinate and synchronize behavioural responses at high cell densities. Autoinducer 2 (AI-2) is the only known quorum-sensing molecule produced by Escherichia coli but its physiological role remains elusive, although it is known to regulate biofilm formation and virulence in other bacterial species. Here we show that chemotaxis towards self-produced AI-2 can mediate collective behaviour—autoaggregation—of E. coli. Autoaggregation requires motility and is strongly enhanced by chemotaxis to AI-2 at physiological cell densities. These effects are observed regardless whether cell–cell interactions under particular growth conditions are mediated by the major E. coli adhesin (antigen 43) or by curli fibres. Furthermore, AI-2-dependent autoaggregation enhances bacterial stress resistance and promotes biofilm formation.

2021 ◽  
Vol 9 (2) ◽  
pp. 386
Author(s):  
Sooyeon Song ◽  
Thomas K. Wood

Autoinducer 2 (AI-2) is a ubiquitous metabolite but, instead of acting as a “universal signal,” relatively few phenotypes have been associated with it, and many scientists believe AI-2 is often a metabolic byproduct rather than a signal. Here, the aim is to present evidence that AI-2 influences both biofilm formation and motility (swarming and chemotaxis), using Escherichia coli as the model system, to establish AI-2 as a true signal with an important physiological role in this bacterium. In addition, AI-2 signaling is compared to the other primary signal of E. coli, indole, and it is shown that they have opposite effects on biofilm formation and virulence.


2017 ◽  
Vol 84 (5) ◽  
Author(s):  
Leanid Laganenka ◽  
Victor Sourjik

ABSTRACTBiofilms 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 byEnterococcus faecalisandEscherichia coli. Our results demonstrate that AI-2 produced byE. faecalispromotes collective behaviors ofE. coliat lower cell densities, enhancing autoaggregation ofE. colibut 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 bothE. coliandE. faecalis.IMPORTANCEThe 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 coliandEnterococcus faecalis. We show that active production of AI-2 byE. faecalisallowsE. colito perform collective behaviors at low cell densities. Additionally, AI-2- and chemotaxis-dependent coaggregation withE. faecaliscreates nucleation zones for rapid growth ofE. colimicrocolonies in mixed biofilms and enhances the stress resistance of both species.


2008 ◽  
Vol 190 (18) ◽  
pp. 6170-6177 ◽  
Author(s):  
Linda D. Rankin ◽  
Diane M. Bodenmiller ◽  
Jonathan D. Partridge ◽  
Shirley F. Nishino ◽  
Jim C. Spain ◽  
...  

ABSTRACT Chromatin immunoprecipitation and microarray (ChIP-chip) analysis showed that the nitric oxide (NO)-sensitive repressor NsrR from Escherichia coli binds in vivo to the promoters of the tynA and feaB genes. These genes encode the first two enzymes of a pathway that is required for the catabolism of phenylethylamine (PEA) and its hydroxylated derivatives tyramine and dopamine. Deletion of nsrR caused small increases in the activities of the tynA and feaB promoters in cultures grown on PEA. Overexpression of nsrR severely retarded growth on PEA and caused a marked repression of the tynA and feaB promoters. Both the growth defect and the promoter repression were reversed in the presence of a source of NO. These results are consistent with NsrR mediating repression of the tynA and feaB genes by binding (in an NO-sensitive fashion) to the sites identified by ChIP-chip. E. coli was shown to use 3-nitrotyramine as a nitrogen source for growth, conditions which partially induce the tynA and feaB promoters. Mutation of tynA (but not feaB) prevented growth on 3-nitrotyramine. Growth yields, mutant phenotypes, and analyses of culture supernatants suggested that 3-nitrotyramine is oxidized to 4-hydroxy-3-nitrophenylacetate, with growth occurring at the expense of the amino group of 3-nitrotyramine. Accordingly, enzyme assays showed that 3-nitrotyramine and its oxidation product (4-hydroxy-3-nitrophenylacetaldehyde) could be oxidized by the enzymes encoded by tynA and feaB, respectively. The results suggest that an additional physiological role of the PEA catabolic pathway is to metabolize nitroaromatic compounds that may accumulate in cells exposed to NO.


2014 ◽  
Vol 81 (4) ◽  
pp. 1477-1489 ◽  
Author(s):  
Nancy Weiland-Bräuer ◽  
Nicole Pinnow ◽  
Ruth A. Schmitz

ABSTRACTTwo reporter strains were established to identify novel biomolecules interfering with bacterial communication (quorum sensing [QS]). The basic design of theseEscherichia coli-based systems comprises a gene encoding a lethal protein fused to promoters induced in the presence of QS signal molecules. Consequently, theseE. colistrains are unable to grow in the presence of the respective QS signal molecules unless a nontoxic QS-interfering compound is present. The first reporter strain designed to detect autoinducer-2 (AI-2)-interfering activities (AI2-QQ.1) contained theE. coliccdBlethal gene under the control of theE. colilsrApromoter. The second reporter strain (AI1-QQ.1) contained theVibrio fischeriluxIpromoter fused to theccdBgene to detect interference with acyl-homoserine lactones. Bacteria isolated from the surfaces of several marine eukarya were screened for quorum-quenching (QQ) activities using the established reporter systems AI1-QQ.1 and AI2-QQ.1. Out of 34 isolates, two interfered with acylated homoserine lactone (AHL) signaling, five interfered with AI-2 QS signaling, and 10 were demonstrated to interfere with both signal molecules. Open reading frames (ORFs) conferring QQ activity were identified for three selected isolates (Photobacteriumsp.,Pseudoalteromonassp., andVibrio parahaemolyticus). Evaluation of the respective heterologously expressed and purified QQ proteins confirmed their ability to interfere with the AHL and AI-2 signaling processes.


2008 ◽  
Vol 191 (4) ◽  
pp. 1248-1257 ◽  
Author(s):  
Yun Wu ◽  
F. Wayne Outten

ABSTRACT Biofilm formation is a complex developmental process regulated by multiple environmental signals. In addition to other nutrients, the transition metal iron can also regulate biofilm formation. Iron-dependent regulation of biofilm formation varies by bacterial species, and the exact regulatory pathways that control iron-dependent biofilm formation are often unknown or only partially characterized. To address this gap in our knowledge, we examined the role of iron availability in regulating biofilm formation in Escherichia coli. The results indicate that biofilm formation is repressed under low-iron conditions in E. coli. Furthermore, a key iron regulator, IscR, controls biofilm formation in response to changes in cellular Fe-S homeostasis. IscR regulates the FimE recombinase to control expression of type I fimbriae in E. coli. We propose that iron-dependent regulation of FimE via IscR leads to decreased surface attachment and biofilm dispersal under iron-limiting conditions.


2007 ◽  
Vol 189 (16) ◽  
pp. 6011-6020 ◽  
Author(s):  
Jun Li ◽  
Can Attila ◽  
Liang Wang ◽  
Thomas K. Wood ◽  
James J. Valdes ◽  
...  

ABSTRACT The regulatory network for the uptake of Escherichia coli autoinducer 2 (AI-2) is comprised of a transporter complex, LsrABCD; its repressor, LsrR; and a cognate signal kinase, LsrK. This network is an integral part of the AI-2 quorum-sensing (QS) system. Because LsrR and LsrK directly regulate AI-2 uptake, we hypothesized that they might play a wider role in regulating other QS-related cellular functions. In this study, we characterized physiological changes due to the genomic deletion of lsrR and lsrK. We discovered that many genes were coregulated by lsrK and lsrR but in a distinctly different manner than that for the lsr operon (where LsrR serves as a repressor that is derepressed by the binding of phospho-AI-2 to the LsrR protein). An extended model for AI-2 signaling that is consistent with all current data on AI-2, LuxS, and the LuxS regulon is proposed. Additionally, we found that both the quantity and architecture of biofilms were regulated by this distinct mechanism, as lsrK and lsrR knockouts behaved identically. Similar biofilm architectures probably resulted from the concerted response of a set of genes including flu and wza, the expression of which is influenced by lsrRK. We also found for the first time that the generation of several small RNAs (including DsrA, which was previously linked to QS systems in Vibrio harveyi) was affected by LsrR. Our results suggest that AI-2 is indeed a QS signal in E. coli, especially when it acts through the transcriptional regulator LsrR.


2006 ◽  
Vol 72 (11) ◽  
pp. 7294-7300 ◽  
Author(s):  
Pieter Moons ◽  
Rob Van Houdt ◽  
Abram Aertsen ◽  
Kristof Vanoirbeek ◽  
Yves Engelborghs ◽  
...  

ABSTRACT We have previously characterized the N-acyl-l-homoserine lactone-based quorum-sensing system of the biofilm isolate Serratia plymuthica RVH1. Here we investigated the role of quorum sensing and of quorum-sensing-dependent production of an antimicrobial compound (AC) on biofilm formation by RVH1 and on the cocultivation of RVH1 and Escherichia coli in planktonic cultures or in biofilms. Biofilm formation of S. plymuthica was not affected by the knockout of splI or splR, the S. plymuthica homologs of the luxI or luxR quorum-sensing gene, respectively, or by the knockout of AC production. E. coli grew well in mixed broth culture with RVH1 until the latter reached 8.5 to 9.5 log CFU/ml, after which the E. coli colony counts steeply declined. In comparison, only a very small decline occurred in cocultures with the S. plymuthica AC-deficient and splI mutants. Complementation with exogenous N-hexanoyl-l-homoserine lactone rescued the wild-type phenotype of the splI mutant. The splR knockout mutant also induced a steep decline of E. coli, consistent with its proposed function as a repressor of quorum-sensing-regulated genes. The numbers of E. coli in 3-day-old mixed biofilms followed a similar pattern, being higher with S. plymuthica deficient in SplI or AC production than with wild-type S. plymuthica, the splR mutant, or the splI mutant in the presence of N-hexanoyl-l-homoserine lactone. Confocal laser scanning microscopic analysis of mixed biofilms established with strains producing different fluorescent proteins showed that E. coli microcolonies were less developed in the presence of RVH1 than in the presence of the AC-deficient mutant.


2018 ◽  
Vol 475 (8) ◽  
pp. 1491-1506 ◽  
Author(s):  
Benjamin M. Fontaine ◽  
Kevin S. Martin ◽  
Jennifer M. Garcia-Rodriguez ◽  
Claire Jung ◽  
Laura Briggs ◽  
...  

Regulation of nucleotide and nucleoside concentrations is critical for faithful DNA replication, transcription, and translation in all organisms, and has been linked to bacterial biofilm formation. Unusual 2′,3′-cyclic nucleotide monophosphates (2′,3′-cNMPs) recently were quantified in mammalian systems, and previous reports have linked these nucleotides to cellular stress and damage in eukaryotes, suggesting an intriguing connection with nucleotide/nucleoside pools and/or cyclic nucleotide signaling. This work reports the first quantification of 2′,3′-cNMPs in Escherichia coli and demonstrates that 2′,3′-cNMP levels in E. coli are generated specifically from RNase I-catalyzed RNA degradation, presumably as part of a previously unidentified nucleotide salvage pathway. Furthermore, RNase I and 2′,3′-cNMP levels are demonstrated to play an important role in controlling biofilm formation. This work identifies a physiological role for cytoplasmic RNase I and constitutes the first progress toward elucidating the biological functions of bacterial 2′,3′-cNMPs.


2001 ◽  
Vol 183 (18) ◽  
pp. 5239-5247 ◽  
Author(s):  
Matthew P. DeLisa ◽  
Chi-Fang Wu ◽  
Liang Wang ◽  
James J. Valdes ◽  
William E. Bentley

ABSTRACT Bacterial cell-to-cell communication facilitates coordinated expression of specific genes in a growth rate-II and cell density-dependent manner, a process known as quorum sensing. While the discovery of a diffusible Escherichia coli signaling pheromone, termed autoinducer 2 (AI-2), has been made along with several quorum sensing genes, the overall number and coordination of genes controlled by quorum sensing through the AI-2 signal has not been studied systematically. We investigated global changes in mRNA abundance elicited by the AI-2 signaling molecule through the use of aluxS mutant that was unable to synthesize AI-2. Remarkably, 242 genes, comprising ca. 5.6% of the E. coli genome, exhibited significant transcriptional changes (either induction or repression) in response to a 300-fold AI-2 signaling differential, with many of the identified genes displaying high induction levels (more than fivefold). Significant induction of ygeV, a putative ς54-dependent transcriptional activator, andyhbH, a ς54 modulating protein, suggests ς54 may be involved in E. coli quorum sensing.


2011 ◽  
Vol 64 (6) ◽  
pp. 1284-1290 ◽  
Author(s):  
Sheng-Hua Zhang ◽  
Xin Yu ◽  
Feng Guo ◽  
Zhuo-ying Wu

Quorum sensing (QS) is a form of microbial communication that relies on small signal molecules to regulate group behaviors such as biofilm formation in response to population density. In this study, we attempted to apply the paradigm of bacterial QS to aerobic granular sludge (AGS) formation for wastewater treatment. An essential element of interspecies QS signals, boron, was added to a sequencing batch reactor (SBR) to stimulate AGS growth. Bioassays elaborated the activity of autoinducer-2 (AI-2). We found that boron accelerated AGS growth, resulting in improved settlement performance and increased biomass in the SBR. During continuous SBR operation, the AGS showed an obvious increase in AI-2 activity, which implies that interspecies QS was closely associated with AGS formation. Analysis of EPS showed that boron stimulated tryptophan production, and increased the hydrophobia of AGS. From these results, it was speculated that the addition of boron may have promoted the formation of boron complexed to (R)-4, 5-dihydroxy-2,3-pentanedione (DPD) as the precursor of AI-2, which resulted in accelerated interspecies QS. The results also suggested QS as a novel regulation target for the biogranulation process, such as AGS formation.


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