Opposite effects of cefoperazone and ceftazidime on S-ribosylhomocysteine lyase/autoinducer-2 quorum sensing and biofilm formation by an Escherichia coli clinical isolate

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.

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Autoinducer 2 Controls Biofilm Formation in Escherichia coli through a Novel Motility Quorum-Sensing Regulator (MqsR, B3022)

Journal of Bacteriology ◽

10.1128/jb.188.1.305-316.2006 ◽

2006 ◽

Vol 188 (1) ◽

pp. 305-316 ◽

Cited By ~ 366

Author(s):

Andrés F. González Barrios ◽

Rongjun Zuo ◽

Yoshifumi Hashimoto ◽

Li Yang ◽

William E. Bentley ◽

...

Keyword(s):

Escherichia Coli ◽

Quorum Sensing ◽

Continuous Flow ◽

Biofilm Formation ◽

Type Strain ◽

Wild Type Strain ◽

Wild Type ◽

Flow Cells ◽

Autoinducer 2 ◽

K 12

ABSTRACT The cross-species bacterial communication signal autoinducer 2 (AI-2), produced by the purified enzymes Pfs (nucleosidase) and LuxS (terminal synthase) from S-adenosylhomocysteine, directly increased Escherichia coli biofilm mass 30-fold. Continuous-flow cells coupled with confocal microscopy corroborated these results by showing the addition of AI-2 significantly increased both biofilm mass and thickness and reduced the interstitial space between microcolonies. As expected, the addition of AI-2 to cells which lack the ability to transport AI-2 (lsr null mutant) failed to stimulate biofilm formation. Since the addition of AI-2 increased cell motility through enhanced transcription of five motility genes, we propose that AI-2 stimulates biofilm formation and alters its architecture by stimulating flagellar motion and motility. It was also found that the uncharacterized protein B3022 regulates this AI-2-mediated motility and biofilm phenotype through the two-component motility regulatory system QseBC. Deletion of b3022 abolished motility, which was restored by expressing b3022 in trans. Deletion of b3022 also decreased biofilm formation significantly, relative to the wild-type strain in three media (46 to 74%) in 96-well plates, as well as decreased biomass (8-fold) and substratum coverage (19-fold) in continuous-flow cells with minimal medium (growth rate not altered and biofilm restored by expressing b3022 in trans). Deleting b3022 changed the wild-type biofilm architecture from a thick (54-μm) complex structure to one that contained only a few microcolonies. B3022 positively regulates expression of qseBC, flhD, fliA, and motA, since deleting b3022 decreased their transcription by 61-, 25-, 2.4-, and 18-fold, respectively. Transcriptome analysis also revealed that B3022 induces crl (26-fold) and flhCD (8- to 27-fold). Adding AI-2 (6.4 μM) increased biofilm formation of wild-type K-12 MG1655 but not that of the isogenic b3022, qseBC, fliA, and motA mutants. Adding AI-2 also increased motA transcription for the wild-type strain but did not stimulate motA transcription for the b3022 and qseB mutants. Together, these results indicate AI-2 induces biofilm formation in E. coli through B3022, which then regulates QseBC and motility; hence, b3022 has been renamed the motility quorum-sensing regulator gene (the mqsR gene).

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Autoinducer-2 Triggers the Oxidative Stress Response in Mycobacterium avium, Leading to Biofilm Formation

Applied and Environmental Microbiology ◽

10.1128/aem.02066-07 ◽

2008 ◽

Vol 74 (6) ◽

pp. 1798-1804 ◽

Cited By ~ 51

Author(s):

Henriette Geier ◽

Serge Mostowy ◽

Gerard A. Cangelosi ◽

Marcel A. Behr ◽

Timothy E. Ford

Keyword(s):

Oxidative Stress ◽

Stress Response ◽

Quorum Sensing ◽

Mycobacterium Avium ◽

Biofilm Formation ◽

Transcriptional Response ◽

Opportunistic Pathogen ◽

Environmental Stresses ◽

Oxidative Stress Response ◽

Autoinducer 2

ABSTRACT Mycobacterium avium is an environmental organism and opportunistic pathogen with inherent resistance to drugs, environmental stresses, and the host immune response. To adapt to these disparate conditions, M. avium must control its transcriptional response to environmental cues. M. avium forms biofilms in various environmental settings, including drinking water pipes and potable water reservoirs. In this study, we investigated the role of the universal signaling molecule autoinducer-2 (AI-2) in biofilm formation by M. avium. The addition of the compound to planktonic M. avium cultures resulted in increased biofilm formation. Microarray and reverse transcriptase PCR studies revealed an upregulation of the oxidative stress response upon addition of AI-2. This suggests that the response to AI-2 might be related to oxidative stress, rather than quorum sensing. Consistent with this model, addition of hydrogen peroxide, a known stimulus of the oxidative stress response, to M. avium cultures resulted in elevated biofilm formation. These results suggest that AI-2 does not act as a quorum-sensing signal in M. avium. Instead, biofilm formation is triggered by environmental stresses of biotic and abiotic origins and AI-2 may exert effects on that level.

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YdgG (TqsA) Controls Biofilm Formation in Escherichia coli K-12 through Autoinducer 2 Transport

Journal of Bacteriology ◽

10.1128/jb.188.2.587-598.2006 ◽

2006 ◽

Vol 188 (2) ◽

pp. 587-598 ◽

Cited By ~ 128

Author(s):

Moshe Herzberg ◽

Ian K. Kaye ◽

Wolfgang Peti ◽

Thomas K. Wood

Keyword(s):

Escherichia Coli ◽

Biofilm Formation ◽

Acid Production ◽

Polysialic Acid ◽

Fold Increase ◽

Uncharacterized Protein ◽

Biofilm Thickness ◽

Autoinducer 2 ◽

Membrane Spanning ◽

K 12

ABSTRACT YdgG is an uncharacterized protein that is induced in Escherichia coli biofilms. Here it is shown that deletion of ydgG decreased extracellular and increased intracellular concentrations of autoinducer 2 (AI-2); hence, YdgG enhances transport of AI-2. Consistent with this hypothesis, deletion of ydgG resulted in a 7,000-fold increase in biofilm thickness and 574-fold increase in biomass in flow cells. Also consistent with the hypothesis, deletion of ydgG increased cell motility by increasing transcription of flagellar genes (genes induced by AI-2). By expressing ydgG in trans, the wild-type phenotypes for extracellular AI-2 activity, motility, and biofilm formation were restored. YdgG is also predicted to be a membrane-spanning protein that is conserved in many bacteria, and it influences resistance to several antimicrobials, including crystal violet and streptomycin (this phenotype could also be complemented). Deletion of ydgG also caused 31% of the bacterial chromosome to be differentially expressed in biofilms, as expected, since AI-2 controls hundreds of genes. YdgG was found to negatively modulate expression of flagellum- and motility-related genes, as well as other known products essential for biofilm formation, including operons for type 1 fimbriae, autotransporter protein Ag43, curli production, colanic acid production, and production of polysaccharide adhesin. Eighty genes not previously related to biofilm formation were also identified, including those that encode transport proteins (yihN and yihP), polysialic acid production (gutM and gutQ), CP4-57 prophage functions (yfjR and alpA), methionine biosynthesis (metR), biotin and thiamine biosynthesis (bioF and thiDFH), anaerobic metabolism (focB, hyfACDR, ttdA, and fumB), and proteins with unknown function (ybfG, yceO, yjhQ, and yjbE); 10 of these genes were verified through mutation to decrease biofilm formation by 40% or more (yfjR, bioF, yccW, yjbE, yceO, ttdA, fumB, yjiP, gutQ, and yihR). Hence, it appears YdgG controls the transport of the quorum-sensing signal AI-2, and so we suggest the gene name tqsA.

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CONDITIONS AFFECTING AUTOINDUCER-2-BASED QUORUM-SENSING OF ESCHERICHIA COLI O157:H7 ON FRESH BEEF

Journal of Food Safety ◽

10.1111/j.1745-4565.2008.00133.x ◽

2008 ◽

Vol 28 (4) ◽

pp. 587-600 ◽

Cited By ~ 1

Author(s):

Y. YOON ◽

J.N. SOFOS

Keyword(s):

Escherichia Coli ◽

Quorum Sensing ◽

Escherichia Coli O157 ◽

Autoinducer 2

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Quorum sensing signal autoinducer-2 promotes root colonization of Bacillus velezensis SQR9 by affecting biofilm formation and motility

Applied Microbiology and Biotechnology ◽

10.1007/s00253-020-10713-w ◽

2020 ◽

Vol 104 (16) ◽

pp. 7177-7185

Author(s):

Qin Xiong ◽

Di Liu ◽

Huihui Zhang ◽

Xiaoyan Dong ◽

Guishan Zhang ◽

...

Keyword(s):

Quorum Sensing ◽

Biofilm Formation ◽

Root Colonization ◽

Bacillus Velezensis ◽

Autoinducer 2

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Quorum sensing is crucial to Escherichia coli O157:H7 biofilm formation under static or very slow laminar flow conditions

BioChip Journal ◽

10.1007/s13206-016-0310-9 ◽

2016 ◽

Vol 10 (3) ◽

pp. 241-249 ◽

Cited By ~ 5

Author(s):

Jeesun Lim ◽

Kang-Mu Lee ◽

Chan Yong Park ◽

Han Vit Kim ◽

Younghoon Kim ◽

...

Keyword(s):

Escherichia Coli ◽

Quorum Sensing ◽

Laminar Flow ◽

Biofilm Formation ◽

Escherichia Coli O157 ◽

Flow Conditions ◽

Laminar Flow Conditions

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Autoinducer-2 of quorum sensing is involved in cell damage caused by avian pathogenic Escherichia coli

Microbial Pathogenesis ◽

10.1016/j.micpath.2016.08.033 ◽

2016 ◽

Vol 99 ◽

pp. 247-252 ◽

Cited By ~ 4

Author(s):

Zhen-Qiang Cui ◽

Zong-Mei Wu ◽

Yun-Xing Fu ◽

Dao-Xiu Xu ◽

Xun Guo ◽

...

Keyword(s):

Escherichia Coli ◽

Quorum Sensing ◽

Cell Damage ◽

Avian Pathogenic Escherichia Coli ◽

Autoinducer 2 ◽

Pathogenic Escherichia Coli

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Quorum Sensing in Escherichia coli Is Signaled by AI-2/LsrR: Effects on Small RNA and Biofilm Architecture

Journal of Bacteriology ◽

10.1128/jb.00014-07 ◽

2007 ◽

Vol 189 (16) ◽

pp. 6011-6020 ◽

Cited By ~ 135

Author(s):

Jun Li ◽

Can Attila ◽

Liang Wang ◽

Thomas K. Wood ◽

James J. Valdes ◽

...

Keyword(s):

Escherichia Coli ◽

Quorum Sensing ◽

Small Rnas ◽

Current Data ◽

Extended Model ◽

Cellular Functions ◽

E Coli ◽

Autoinducer 2 ◽

Distinct Mechanism ◽

First Time

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.

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