Selection for non-specific adhesion is a driver of FimH evolution increasing Escherichia coli biofilm capacity

Bacterial interactions with surfaces rely on the coordinated expression and interplay of surface exposed adhesion factors. However, how bacteria dynamically modulate their vast repertoire of adhesins to achieve surface colonization is not yet well-understood. We used experimental evolution and positive selection for improved adhesion to investigate how an initially poorly adherent Escherichia coli strain increased its adhesion capacities to abiotic surfaces. We showed that all identified evolved clones acquired mutations located almost exclusively in the lectin domain of fimH, the gene coding for the alpha-D-mannose-specific tip adhesin of type 1 fimbriae. While most of these fimH mutants showed reduced mannose-binding ability, they all displayed enhanced binding to abiotic surfaces, indicating a trade-off between FimH-mediated specific and non-specific adhesion properties. Several of the identified mutations were already reported in FimH lectin domain of pathogenic and environmental E. coli, suggesting that, beyond patho-adaptation, FimH microevolution favoring non-specific surface adhesion could constitute a selective advantage for natural E. coli isolates. Consistently, although E. coli deleted for the fim operon still evolves an increased adhesion capacity, mutants selected in the ∆fim background are outcompeted by fimH mutants revealing clonal interference for adhesion. Our study therefore provides insights into the plasticity of E. coli adhesion potential and shows that evolution of type 1 fimbriae is a major driver of the adaptation of natural E. coli to colonization.

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Role of the ceramide-signaling pathway in cytokine responses to P-fimbriated Escherichia coli.

Journal of Experimental Medicine ◽

10.1084/jem.183.3.1037 ◽

1996 ◽

Vol 183 (3) ◽

pp. 1037-1044 ◽

Cited By ~ 115

Author(s):

M Hedlund ◽

M Svensson ◽

A Nilsson ◽

R D Duan ◽

C Svanborg

Keyword(s):

Escherichia Coli ◽

Signaling Pathway ◽

Kinase Inhibitors ◽

Human Kidney ◽

Cytokine Response ◽

Protein Kinase Inhibitors ◽

E Coli ◽

Type 1 Fimbriae ◽

Outer Leaflet

Escherichia coli express fimbriae-associated adhesins through which they attach to mucosal cells and activate a cytokine response. The receptors for E. coli P fimbriae are the globoseries of glycosphingolipids; Gal alpha 1-->4Gal beta-containing oligosaccharides bound to ceramide in the outer leaflet of the lipid bilayer. The receptors for type 1 fimbriae are mannosylated glycoproteins rather than glycolipids. This study tested the hypothesis that P-fimbriated E. coli elicit a cytokine response through the release of ceramide in the receptor-bearing cell. We used the A498 human kidney cell line, which expressed functional receptors for P and type 1 fimbriae and secreted higher levels of interleukin (IL)-6 when exposed to the fimbriated strains than to isogenic nonfimbriated controls. P-fimbriated E. coli caused the release of ceramide and increased the phosphorylation of ceramide to ceramide 1-phosphate. The IL-6 response to P-fimbriated E. coli was reduced by inhibitors of serine/threonine kinases but not by other protein kinase inhibitors. In contrast, ceramide levels were not influenced by type 1-fimbriated E. coli, and the IL-6 response was insensitive to the serine/threonine kinase inhibitors. These results demonstrate that the ceramide-signaling pathway is activated by P-fimbriated E. coli, and that the receptor specificity of the P fimbriae influences this process. We propose that this activation pathway contributes to the cytokine induction by P-fimbriated E. coli in epithelial cells.

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Uropathogenic Escherichia coli Triggers Oxygen-Dependent Apoptosis in Human Neutrophils through the Cooperative Effect of Type 1 Fimbriae and Lipopolysaccharide

Infection and Immunity ◽

10.1128/iai.72.8.4570-4578.2004 ◽

2004 ◽

Vol 72 (8) ◽

pp. 4570-4578 ◽

Cited By ~ 39

Author(s):

Robert Blomgran ◽

Limin Zheng ◽

Olle Stendahl

Keyword(s):

Escherichia Coli ◽

Urinary Tract ◽

Human Neutrophils ◽

Dependent Manner ◽

E Coli ◽

Type 1 Fimbriae ◽

The Difference ◽

Tract Infections ◽

Neutrophil Survival

ABSTRACT Type 1 fimbriae are the most commonly expressed virulence factor on uropathogenic Escherichia coli. In addition to promoting avid bacterial adherence to the uroepithelium and enabling colonization, type 1 fimbriae recruit neutrophils to the urinary tract as an early inflammatory response. Using clinical isolates of type 1 fimbriated E. coli and an isogenic type 1 fimbria-negative mutant (CN1016) lacking the FimH adhesin, we investigated if these strains could modulate apoptosis in human neutrophils. We found that E. coli expressing type 1 fimbriae interacted with neutrophils in a mannose- and lipopolysaccharide (LPS)-dependent manner, leading to apoptosis which was triggered by the intracellular generation of reactive oxygen species. This induced neutrophil apoptosis was abolished by blocking FimH-mediated attachment, by inhibiting NADPH oxidase activation, or by neutralizing LPS. In contrast, CN1016, which did not adhere to or activate the respiratory burst of neutrophils, delayed the spontaneous apoptosis in an LPS-dependent manner. This delayed apoptosis could be mimicked by adding purified LPS and was also observed by using fimbriated bacteria in the presence of d-mannose. These results suggest that LPS is required for E. coli to exert both pro- and antiapoptotic effects on neutrophils and that the difference in LPS presentation (i.e., with or without fimbriae) determines the outcome. The present study showed that there is a fine-tuned balance between type 1 fimbria-induced and LPS-mediated delay of apoptosis in human neutrophils, in which altered fimbrial expression on uropathogenic E. coli determines the neutrophil survival and the subsequent inflammation during urinary tract infections.

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Adhesion of enteropathogenic, enterotoxigenic and commensal Escherichia coli to the Major Zymogen Granule Membrane Glycoprotein 2

Applied and Environmental Microbiology ◽

10.1128/aem.02279-21 ◽

2022 ◽

Author(s):

Christin Bartlitz ◽

Rafał Kolenda ◽

Jarosław Chilimoniuk ◽

Krzysztof Grzymajło ◽

Stefan Rödiger ◽

...

Keyword(s):

Escherichia Coli ◽

Host Specificity ◽

Pathogenic Bacteria ◽

Cell Receptor ◽

Membrane Glycoprotein ◽

Zymogen Granule ◽

E Coli ◽

Type 1 Fimbriae ◽

Granule Membrane

Pathogenic bacteria, such as enteropathogenic (EPEC) and enterotoxigenic Escherichia coli (ETEC), cause diarrhea in mammals. In particular, E. coli colonize and infect the gastrointestinal tract via type 1 fimbriae (T1F). Here the major zymogen granule membrane glycoprotein 2 (GP2) acts as host cell receptor. GP2 is also secreted by the pancreas and various mucous glands, interacting with luminal type 1 fimbriae-positive E. coli . It is unknown whether GP2 isoforms demonstrate specific E. coli pathotype binding. In this study, we investigated interactions of human, porcine and bovine EPEC, ETEC as well as commensal E. coli isolates with human, porcine and bovine GP2. We first defined pathotype- and host-associated FimH variants. Secondly, we could prove that GP2 isoforms bound to FimH variants to varying degrees. However, the GP2-FimH interactions did not seem to be influenced by the host specificity of E. coli . In contrast, soluble GP2 affected ETEC infection and phagocytosis rates of macrophages. Pre-incubation of ETEC pathotype with GP2 reduced infection of cell lines. Furthermore, pre-incubation of E. coli with GP2 improved the phagocytosis rate of macrophages. Our findings suggest that GP2 plays a role in the defense against E. coli infection and in the corresponding host immune response. IMPORTANCE Infection by pathogenic bacteria such as certain Escherichia coli pathotypes results in diarrhea in mammals. Pathogens, including zoonotic agents, can infect different hosts or show host-specificity. There are Escherichia coli strains which are frequently transmitted between humans and animals, whereas other Escherichia coli strains tend to colonize only one host. This host-specificity is still not fully understood. We show that glycoprotein 2 is a selective receptor for particular Escherichia coli strains or variants of the adhesin FimH but not a selector for a species-specific Escherichia coli group. We demonstrate that GP2 is involved in the regulation of colonization and infection and thus represents a molecule of interest for the prevention or treatment of disease.

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Inactivation of ibeA and ibeT Results in Decreased Expression of Type 1 Fimbriae in Extraintestinal Pathogenic Escherichia coli Strain BEN2908

Infection and Immunity ◽

10.1128/iai.00334-08 ◽

2008 ◽

Vol 76 (9) ◽

pp. 4129-4136 ◽

Cited By ~ 29

Author(s):

Mélanie A. M. Cortes ◽

Julien Gibon ◽

Nathalie K. Chanteloup ◽

Maryvonne Moulin-Schouleur ◽

Philippe Gilot ◽

...

Keyword(s):

Escherichia Coli ◽

Wild Type Strain ◽

Coli Strain ◽

Wild Type ◽

Adhesive Properties ◽

Type 1 Fimbriae ◽

Pathogenic Escherichia Coli ◽

Genes Encoding

ABSTRACT IbeA in extraintestinal pathogenic Escherichia coli (ExPEC) strains was previously described for its role in invasion. Here we investigated the role of IbeA and IbeT, encoded by a gene located downstream of ibeA, in the adhesion of the avian ExPEC strain BEN2908 to human brain microvascular endothelial cells (HBMEC). The ΔibeA mutant was less adhesive to HBMEC than the wild-type strain BEN2908 was. Because strain BEN2908 also expresses type 1 fimbriae, we measured the adhesion specifically due to IbeA by comparing the adhesive properties of a Δfim derivative of strain BEN2908 to those of a double Δfim ΔibeA mutant. No differences were observed, indicating that the reduction of adhesion in BEN2908 ΔibeA could be due to a decrease in type 1 fimbria expression. We indeed showed that the decreased adhesion of BEN2908 ΔibeA was correlated with a decrease in type 1 fimbria expression. Accordingly, more bacteria had a fim promoter orientated in the off position in a culture of BEN2908 ΔibeA than in a culture of BEN2908. Expression of fimB and fimE, two genes encoding recombinases participating in controlling the orientation of the fim promoter, was decreased in BEN2908 ΔibeA. A reduction of type 1 fimbria expression due to a preferential orientation of the fim promoter in the off position was also seen in an ibeT mutant of strain BEN2908. We finally suggest a role for IbeA and IbeT in modulating the expression of type 1 fimbriae through an as yet unknown mechanism.

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Type 1 Fimbriation and Its Phase Switching in Diarrheagenic Escherichia coli Strains

Clinical and Diagnostic Laboratory Immunology ◽

10.1128/cdli.8.3.489-495.2001 ◽

2001 ◽

Vol 8 (3) ◽

pp. 489-495 ◽

Cited By ~ 15

Author(s):

Ken-Ichiro Iida ◽

Yoshimitsu Mizunoe ◽

Sun Nyunt Wai ◽

Shin-Ichi Yoshida

Keyword(s):

Escherichia Coli ◽

Invertible Element ◽

Nucleotide Sequence Analysis ◽

Phase Variable ◽

Phase Switching ◽

E Coli ◽

Static Culture ◽

Type 1 Fimbriae ◽

K 12

ABSTRACT Type 1 fimbriae can be expressed by most Escherichia coli strains and mediate mannose-sensitive (MS) adherence to mammalian epithelial cells. However, the role of type 1 fimbriae in enteric pathogenesis has been unclear. Expression of type 1 fimbriae inE. coli is phase variable and is associated with the inversion of a short DNA element (fim switch). Forty-six strains of diarrheagenic E. coli were examined for the expression of type 1 fimbriae. Only four of these strains were originally type 1 fimbriated. Seventeen strains, originally nonfimbriated, expressed type 1 fimbriae in association with off-to-on inversion of the fim switch, after serial passages in static culture. The switching frequencies of these strains, from fimbriate to nonfimbriate, were greater than that of the laboratory strain E. coli K-12. None of the 16 strains of serovar O157:H7 or O157:H− expressed type 1 fimbriae after serial passages in static culture. The nucleotide sequence analysis of thefim switch region revealed that all of the O157:H7 and O157:H− strains had a 16-bp deletion in the invertible element, and the fim switch was locked in the “off” orientation. The results suggest that expression of type 1 fimbriae may be regulated differently in different E. coli pathogens causing enteric infections.

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The Type VI Secretion System Plays a Role in Type 1 Fimbria Expression and Pathogenesis of an Avian Pathogenic Escherichia coli Strain

Infection and Immunity ◽

10.1128/iai.00531-10 ◽

2010 ◽

Vol 78 (12) ◽

pp. 4990-4998 ◽

Cited By ~ 61

Author(s):

Fernanda de Pace ◽

Gerson Nakazato ◽

Alline Pacheco ◽

Jacqueline Boldrin de Paiva ◽

Vanessa Sperandio ◽

...

Keyword(s):

Escherichia Coli ◽

Epithelial Cells ◽

Disease Process ◽

Secretion System ◽

Coli Strain ◽

Economic Losses ◽

Type Vi Secretion System ◽

Type 1 Fimbriae ◽

Type Vi Secretion

ABSTRACT Avian pathogenic Escherichia coli (APEC) strains frequently cause extraintestinal infections and are responsible for significant economic losses in the poultry industry worldwide. APEC isolates are closely related to human extraintestinal pathogenic E. coli (ExPEC) strains and may also act as pathogens for humans. Known APEC virulence factors include adhesins such as type 1 fimbriae and curli, iron acquisition systems, and cytotoxins. Here we show that APEC strain SEPT362, isolated from a septicemic hen, expresses a type VI secretion system (T6SS); causes cytoskeleton rearrangements; and invades epithelial cells, replicates within macrophages, and causes lethal disease in chicks. To assess the contribution of the T6SS to SEPT362 pathogenesis, we generated two mutants, hcp (which encodes a protein suggested to be both secreted and a structural component of the T6SS) and clpV (encoding the T6SS ATPase). Both mutants showed decreased adherence and actin rearrangement on epithelial cells. However, only the hcp mutant presented a mild decrease in its ability to invade epithelial cells, and none of these mutants were defective for intramacrophage replication. Transcriptome studies showed that the level of expression of type 1 fimbriae was decreased in these mutants, which may account for the diminished adhesion and invasion of epithelial cells. The T6SS seems to be important for the disease process, given that both mutants were attenuated for infection in chicks. These results suggest that the T6SS influences the expression of type 1 fimbriae and contributes to APEC pathogenesis.

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Increased Type 1 Fimbrial Expression among Commensal Escherichia coli Isolates in the Murine Cecum following Catabolic Stress

Infection and Immunity ◽

10.1128/iai.67.2.745-753.1999 ◽

1999 ◽

Vol 67 (2) ◽

pp. 745-753 ◽

Cited By ~ 29

Author(s):

Barbara A. Hendrickson ◽

Jun Guo ◽

Robert Laughlin ◽

Yimei Chen ◽

John C. Alverdy

Keyword(s):

Escherichia Coli ◽

Intestinal Epithelium ◽

Tissue Injury ◽

Fold Increase ◽

E Coli ◽

Type 1 Fimbriae ◽

Colon Cell ◽

Colon Cell Line

ABSTRACT Although indigenous bacteria intimately colonize the intestinal mucosa, under normal conditions the intestinal epithelial cell is free of adherent bacteria. Nonetheless, commensal bacteria such asEscherichia coli adhere to and translocate across the intestinal epithelium in association with a number of pathologic states including hemorrhagic shock, immunosuppression, traumatic tissue injury, and lack of enteral feedings. The adhesins involved in the adherence of indigenous E. coli to the intestinal epithelium in vivo following catabolic stress are unknown. We have developed a mouse model to study the bacterial adhesins which mediate the increased intestinal adherence of E. coliafter partial hepatectomy and short-term starvation. Our studies demonstrated that hepatectomy and starvation in the mouse were associated with a 7,500-fold increase in the numbers of E. coli bacteria adhering to the cecum. In addition, erythrocyte agglutination studies, as well as immunostaining of fimbrial preparations and electron micrographs of the bacteria, revealed that surface type 1 fimbriae were more abundant in the commensal E. coli harvested from the ceca of the stressed mice. These E. coli isolates adhered to a mouse colon cell line and injected cecal loops in a mannose-inhibitable manner, which suggests a role for type 1 fimbriae in the adherence of the E. coli isolates to the cecum in vivo following host catabolic stress.

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Effects of ompA Deletion on Expression of Type 1 Fimbriae in Escherichia coli K1 Strain RS218 and on the Association of E. coli with Human Brain Microvascular Endothelial Cells

Infection and Immunity ◽

10.1128/iai.00321-06 ◽

2006 ◽

Vol 74 (10) ◽

pp. 5609-5616 ◽

Cited By ~ 38

Author(s):

Ching-Hao Teng ◽

Yi Xie ◽

Sooan Shin ◽

Francescopaolo Di Cello ◽

Maneesh Paul-Satyaseela ◽

...

Keyword(s):

Escherichia Coli ◽

Endothelial Cells ◽

Human Brain ◽

Microvascular Endothelial Cells ◽

Mrna Levels ◽

Brain Microvascular Endothelial Cells ◽

E Coli ◽

Type 1 Fimbriae ◽

Microvascular Endothelial

ABSTRACT We have previously shown that outer membrane protein A (OmpA) and type 1 fimbriae are the bacterial determinants involved in Escherichia coli K1 binding to human brain microvascular endothelial cells (HBMEC), which constitute the blood-brain barrier. In investigating the role of OmpA in E. coli K1 binding to HBMEC, we showed for the first time that ompA deletion decreased the expression of type 1 fimbriae in E. coli K1. Decreased expression of type 1 fimbriae in the ompA deletion mutant was largely the result of driving the fim promoter toward the type 1 fimbrial phase-OFF orientation. mRNA levels of fimB and fimE were found to be decreased with the OmpA mutant compared to the parent strain. Of interest, the ompA deletion further decreased the abilities of E. coli K1 to bind to and invade HBMEC under the conditions of fixing type 1 fimbria expression in the phase-ON or phase-OFF status. These findings suggest that the decreased ability of the OmpA mutant to interact with HBMEC is not entirely due to its decreased type 1 fimbrial expression and that OmpA and type 1 fimbriae facilitate the interaction of E. coli K1 with HBMEC at least in an additive manner.

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Regulation of Type 1 Fimbriae by Unlinked FimB- and FimE-Like Recombinases in Uropathogenic Escherichia coli Strain CFT073

Infection and Immunity ◽

10.1128/iai.74.2.1072-1083.2006 ◽

2006 ◽

Vol 74 (2) ◽

pp. 1072-1083 ◽

Cited By ~ 60

Author(s):

Andrew Bryan ◽

Paula Roesch ◽

Lindsay Davis ◽

Rebecca Moritz ◽

Shahaireen Pellett ◽

...

Keyword(s):

Escherichia Coli ◽

Sequence Similarity ◽

Epidemiological Survey ◽

Coli Strain ◽

Amino Acid Sequences ◽

Reciprocal Relationship ◽

E Coli ◽

Normal Human ◽

Strain Cft073

ABSTRACT Genomic DNA sequence analysis of the uropathogenic Escherichia coli strain CFT073 revealed that besides the fimB and fimE recombinase genes that control the type 1 pilus fim phase switch, there are three additional fimB- and fimE-like genes: ipuA, ipuB, and ipbA. Alignment of the predicted amino acid sequences showed that the five recombinases range in sequence similarity from 63 to 70%. An epidemiological survey indicates that ipuA and ipuB are present and linked next to the dsdCXA locus in 24 of 67 uropathogenic E. coli strains but are found in only 1 of 15 normal human fecal isolates. The ipbA sequence located next to the betABIT locus was found in 42 of 67 uropathogenic isolates and 8 of 15 of the commensal strains. We show that two of these recombinases, those encoded by ipuA and ipbA, can function at the type 1 pilus fim switch. In a CFT073 deletion mutant lacking all five recombinase genes, recombinant ipuA or ipbA provided in trans inverted the fim element from the off state to the on state. When a fim OFF CFT073 ΔfimBE mutant was used to infect the urinary tracts of mice, a switch to the fim on state was detected within 24 h in bacteria recovered from urine, the bladder, and the kidneys. A fim OFF CFT073 ΔfimBE ipuB ipbA mutant also demonstrated the ability to switch from the fim off state to the on state during mouse infection. CFT073 recombinase mutants derived from isolates in either the fim on or off state showed a reciprocal relationship for motility. Switches from a nonmotile to a motile phenotype and from a fim on to off genotype were observed in fim ON CFT073 ΔfimBE ipuAB ipbA mutants when ipuA or fimB was provided in trans. Together these results indicate that ipuA has fimB-like on-to-off and off-to-on fim switching activity and that ipbA has the ability to switch fim from the off to the on orientation.

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Adhesion of Escherichia Coli to Nanostructured Surfaces and the Role of Type 1 Fimbriae

Nanomaterials ◽

10.3390/nano10112247 ◽

2020 ◽

Vol 10 (11) ◽

pp. 2247

Author(s):

Pawel Kallas ◽

Håvard J Haugen ◽

Nikolaj Gadegaard ◽

John Stormonth-Darling ◽

Mats Hulander ◽

...

Keyword(s):

Escherichia Coli ◽

Urinary Tract ◽

Urinary Tract Infections ◽

Virulence Factor ◽

Wild Type ◽

E Coli ◽

Type 1 Fimbriae ◽

Tract Infections

Bacterial fimbriae are an important virulence factor mediating adhesion to both biotic and abiotic surfaces and facilitating biofilm formation. The expression of type 1 fimbriae of Escherichia coli is a key virulence factor for urinary tract infections and catheter-associated urinary tract infections, which represent the most common nosocomial infections. New strategies to reduce adhesion of bacteria to surfaces is therefore warranted. The aim of the present study was to investigate how surfaces with different nanotopography-influenced fimbriae-mediated adhesion. Surfaces with three different nanopattern surface coverages made in polycarbonate were fabricated by injection molding from electron beam lithography nanopatterned templates. The surfaces were constructed with features of approximately 40 nm width and 25 nm height with 100 nm, 250 nm, and 500 nm interspace distance, respectively. The role of fimbriae type 1-mediated adhesion was investigated using the E. coli wild type BW25113 and ΔfimA (with a knockout of major pilus protein FimA) and ΔfimH (with a knockout of minor protein FimH) mutants. For the surfaces with nanotopography, all strains adhered least to areas with the largest interpillar distance (500 nm). For the E. coli wild type, no difference in adhesion between surfaces without pillars and the largest interpillar distance was observed. For the deletion mutants, increased adhesion was observed for surfaces without pillars compared to surfaces with the largest interpillar distance. The presence of a fully functional type 1 fimbria decreased the bacterial adhesion to the nanopatterned surfaces in comparison to the mutants.

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