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Distribution of chaperone-usher fimbriae and curli fimbriae among uropathogenic Escherichia coli

BMC Microbiology volume 24, Article number: 344 (2024) Cite this article

Abstract

Background

In the present study, we aimed to determine the frequency of the csgA, fimH, mrkD, foc, papaGI, papGII and papGIII genes, to provide and to design fimbrial adhesin gene (FAG) patterns and profiles for the isolated uropathogenic Escherichia coli (UPEC) strains.

Methods

The enrollment of 108 positive urine samples was performed during seven months, between January 2022 and July 2022. The UPEC strains were confirmed through the standard microbiological and biochemical tests. The antimicrobial susceptibility test was performed through the Kirby–Bauer disc diffusion method. Molecular screening of FAGs was done through the polymerase chain reaction technology. The statistical analyses including chi square and Fisher’s exact tests were performed to interpret the obtained results in the present study.

Results

As the main results, the antimicrobial resistance (AMR) patterns,

multi- (MDR) and extensively drug-resistance (XDR) patterns and FAG patterns were designed and provided. fimH (93.3%), csgA (90.4%) and papG (37.5%) (papGII (30.8%)) genes were recognized as the top three FAGs, respectively. Moreover, the frequency of csgA-fimH gene profile was identified as the top FAG pattern (46.2%) among the others. The isolates bearing csgA-fimH gene profile were armed with a versatile of phenotypic AMR patterns. In the current study, 27.8%, 69.4% and 1.9% of the UPEC isolates were detected as extended-spectrum ß-lactamases (ESBLs) producers, MDR and XDR strains, respectively.

Conclusions

In conclusion, detection, providing and designing of patterns and profiles in association with FAGs, AMR feature in UPEC strains give us an effective option to have a successful and influential prevention for both of UTIs initiation and AMR feature.

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Background

Indeed, the urinary tract infections (UTIs) are known as one of the most important infectious diseases, worldwide. In addition, the UTIs are common among both men and women with different age range. Up to date, uropathogenic Escherichia coli (UPEC) and Klebsiella pneumoniae are recognized as the most important Gram-negative bacterial agents of UTIs [1,2,3,4,5,6,7]. The pan-genomic plasticity in bacterial strains of E. coli makes them armed with a wide arsenal of virulence genes (VGs) (e.g., adhesins, siderophores, toxins, etc.) and antibiotic resistance genes (ARGs) to have a successful attachment, colonization, biofilm formation, invasion and dissemination within the human host body [6, 8,9,10]. Thus, bacterial fimbriae and the related fimbrial adhesins in UPEC strains including curli and chaperone-usher fimbriae are effective virulence factors (VFs) which play pivotal role in initiation of bacterial pathogenesis in association with UTIs through adhesion [6, 9,10,11,12]. The amyloid fiber of curli, contributes to bacterial attachment and colonization and this organelle supports the bacterial cells to form strong biofilms. A strong biofilm covers its constructive bacterial cells from death and devastation in exposure to antibiotics; hence, the bacterial cells within a biofilm structure will be changed into resistant cells to antibiotics which leads to appearance of drug-resistant strains [9, 10, 13, 14]. CsgA amyloids act as curli fimbrial major subunit. This extracellular matrix component (CsgA) makes the bacterial cells resistant to antibiotics within the biofilm [13]. Curli fimbriae which are produced through the Curli pathway, participate in all types of UTIs [10]. On the other hand, there are several adhesive fimbriae (including Type 1, Type 3, F1C and P fimbriae) which are produced via the Chaperone-Usher (CU) fimbrial pathway. These adhesive fibers are known as CU fimbriae and are recognized as effective VFs that support UPEC bacterial cells to have successful attachment, colonization, biofilm formation, dissemination and invasion in human host’s urinary system to initiate different types of UTIs pathogenesis [2, 6, 9, 10]. Type 1 fibers are known as effective CU fibers which contribute to invasion, adhesion, colonization and biofilm formation of UPEC bacterial cells upon the human host’s urothelial cells by the adhesin subunit of FimH. The painful signs of UTIs like dysuria is the result of induced inflammatory responses by the attachment of FimH to the huma host’s urothelial receptors. Type 1 fimbriae are common between UPEC and K. pneumonia strains [6, 9, 15,16,17,18]. Type 3 fibers which belong to CU fimbriae are involved in adhesion, colonization and biofilm formation of UPEC and K. pneumonia bacterial cells upon the biotic surface like human host’s urothelial cells and abiotic surfaces like urinary catheters which may lead to catheter-associated UTIs (CAUTIs). The bacterial cells’ attachment to abiotic and biotic surfaces is achieved via the fimbrial adhesin subunit of MrkD. Type 3 fimbriae are normally involved in CAUTIs; however, they can be involved in non-CAUTIs, too [6, 9, 10, 16, 18,19,20]. F1C as another CU fibers are detectable among 30% of the UPCE pathotypes. it seems that F1C fimbriae have cross-talk with type 1 and P fibers. FocH as the adhesin subunit of F1C fiber is involved in bacterial adhesion, colonization and biofilm formation. Although F1C fibers participate in different types of UTIs, they have strong role in cystitis, pyelonephritis and renal failure in association with UTIs [6, 9, 10, 16, 21, 22]. P fibers via their PapG adhesins, contribute to bacterial adhesion upon the urothelial cells and are involved in all types of UTIs pathogenesis. Up to date, four different variants have been detected for PapG subunits including PapGI, PapGII, PapGIII and PapGIV [6, 9,10,11, 23]. PapGI has a pale role in UTIs pathogenesis and the related clinical syndromes while, PapGII is related to pyelonephritis (both in adult females and children), acute prostatitis (in males) and invasive infections which may lead to bacteremia in patients with UTIs [6, 9,10,11, 23]. PapGIII is associated with cystitis both in adults and children while the role and frequency of PapGIV has not been clearly, recorded [11, 24]. In accordance with the aforementioned background, the fimbrial adhesins are considered as bifunctional arsenal for UPEC strains which act as both of VFs and antimicrobial resistant factors (AMRFs). As the raise of antimicrobial resistance (AMR) feature is a global concern, detection and designing of fimbrial adhesin gene (FAG) patterns and profiles together with the AMR-, multi- and extensively drug-resistance patterns and profiles may inspire us to change our treatment procedures rather than the use of antibiotics. In recent years, our global colleagues are trying to provide effective agonists to prevent both of initiation of UTIs and promotion of AMR feature. Thus, in the current investigation the authors aimed to find out the prevalence of FAGs and to provide and to design FAG patterns and profiles, phenotypic AMR patterns and profiles, phenotypic MDR and XDR patterns and profiles for the UPEC isolates. This investigation would be an effective resource for scientists who work in the field of agonists to prevent the initiation of UTIs and to replace them instead of antibiotics and drugs.

Materials and methods

Sample collection

The enrollment of clinical samples of midstream (clean-catch) urines for UPEC in this cross-sectional study was performed from four different labs and hospital during seven months, between January 2022 and July 2022. Because of COVID-19 infection concerns, we requested the laboratories’ technicians and experts not to collect the positive urine samples for UPEC from patients with COVID-19 infection. The anonymous positive urine samples were belonged to 108 in- and out-patients. Only positive cases of urine samples (≥ 105 colony forming units (CFUs)/mL) which were confirmed by the laboratories’ technicians and experts were obtained by the authors. Patients with COVID-19 infection were recognized as exclusion criterion and non-COVID-19 patients with UTIs (≥ 105 colony forming units (CFUs)/mL) were recognized as inclusion criterion. Neither patients nor their information excluding their age range and gender were accessible to us. As everything was anonymous to us, we have no data about the clinical signs and symptoms of the patients and their destinies. Since, all materials excluding the age range and the gender of the patients were anonymous to us and the confirmed positive urine samples were enrolled by the Labs’ and hospital’s technicians and experts no ethical approval was needed for this project. This study was achieved according to the Declaration of Helsinki guidelines. This scientific investigation has been performed under the permission number of DP/97/220 (97/12/12), issued by the Research Council of the Islamic Azad University, Shahr-e-Qods Branch.

Bacterial identification

MacConkey agar (Quelab, Quebec), EMB agar (IBRESCO, Italy) (to obtain typical green metallic colonies of UPEC cells) and blood agar (IBRESCO, Italy) (to enrich bacterial growth) were used to inoculate the specimens. Then, they were incubated at 37 °C during 24 h. In follow, the well-grown bacterial colonies of UPEC were confirmed through the standard microbiological and biochemical tests e.g., Gram staining, SIM, TSI, IMViC (IBRESCO, Italy) and urease hydrolysis (Merck, Germany) [18, 25]. In continue, the Luria–Bertani (LB) culture medium (IBRESCO, Italy) was used to be inoculated by the confirmed bacterial isolates of UPEC. Then, the inoculated culture media were incubated at 37 °C during 24 h. Finally, the well-grown bacterial colonies of UPEC isolates were employed for antimicrobial susceptibility test (AST) and DNA extraction procedures [18, 26].

Antimicrobial susceptibility test (AST)

In the present study, the AST was run on Mueller–Hinton agar (IBRESCO, Italy) in accordance with Kirby–Bauer disc diffusion method [27]. Due to this fact, 14 mono antibiotic discs (Padtan-Teb, Iran) including of aminoglycosides (Amikacin (AN).

(30 μg/disc), Kanamycin (K) (30 μg/disc), Gentamicin (G) (10 μg/disc)), penicillins (Ampicillin (10 μg/disc)), glycols (Chloramphenicol (30 μg /disc)), organophosphonates (Fosfomycin (Phosphomycin) (FOS) (200 μg/disc)), carbapenems (Imipenem (IPM) (10 μg/disc)), tetracyclines (Tetracycline (TE).

(30 μg/disc), nitrofurans (Nitrofurantoin (NFT) (300 μg/disc)), sulfonamides (Trimethoprim-Sulfamethoxazole (Co-trimoxazole) (SXT) (1.25/23.75 μg/disc), fluoroquinolones (Ciprofloxacin (CIP) (5 μg /disc)), cephalosporins (Cefepime (FEP) (30 μg/disc), Ceftazidime (CAZ) (30 μg/disc), Cefotaxime (CTX) (30 μg/disc)) were recruited. The bacterial strain of E. coli ATCC 25922 was employed as the negative control. As Table 2 shows, the AST results were interpreted according to CLSI 2021 [27].

Extended-spectrum beta-lactamases (ESBL) phenotypic detection test

Moreover, the ESBL phenotypic detection test [27] was performed for those isolates which were resistant to one of the cephalosporins such as FEP, CAZ or CTX in AST. In this regard, three combined ß-lactam-ß-lactamase inhibitor discs (Padtan-Teb, Iran) comprising Cefepime + Clavulanate (FEC) (30 μg + 10 μg/disc), Ceftazidime + Clavulanate (CZC) (30 μg + 10 μg/disc) and Cefotaxime + Clavulanate (CTC) (30 μg + 10 μg/disc) were used. I1 was presumed as the diameter of inhibition zone for mono cephalosporin disc and I2 was presumed as the diameter of inhibition zone for combined ß-lactam-ß-lactamase inhibitor disc, then the I2-I1 ≥ 5 mm was recognized as ESBL positive isolate. The bacterial strain of E. coli ATCC 25922 was employed as the negative control. In addition, the Multidrug-resistance (MDR) isolates (nonsusceptibility to ≥ 1 agent in ≥ 3 antimicrobial categories); the Extensively drug-resistant (XDR) isolates (susceptibility limited to ≤ 2 antimicrobial categories); and the Pan drug-resistance (PDR) isolates (nonsusceptibility to entire agents in association with all the antimicrobial categories) were screened in the present study [28, 29].

DNA extraction and polymerase chain reaction

In the present study, the bacterial DNA templates pertaining to 108 clinical UPEC strains were harvested through the boiling method. For this purpose, the well-grown colonies of UPEC isolates on LB agar were suspended within 100 μl RNase- and DNase free double distilled water (ddw). Then, each suspension was boiled (within the water bath) for 10 min. In follow, the boiled suspension was centrifuged at 13,000 rpm for another 10 min. The obtained supernatant, contained harvested DNA templates. The purity and quality of extracted DNA templates were evaluated through NanoDrop™ spectrophotometer. The harvested genomic DNA were kept.

at -20 °C [5, 18, 25, 26]. Then, further molecular procedures were done.

Molecular screening of CU and curli fimbriae genes via PCR technology

In the present study, seven FAGs in association with five fimbriae including curli fimbriae which are known as non-CUF and four CUF involving type 1, type 3, F1C and P fimbriae. In this regard, the applied primers and the related PCR thermal profile are indicated in Table 1.

Table 1 A list of target genes, employed PCR primers and PCR thermal profile
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In the present study, the monoplex PCR was recruited for the target genes of csgA, fimH, mrkD, and foc, separately. The PCR cocktail with a final volume of 25 μL was prepared by adding 12.5 μL Master Mix (2 ×) (Tris- HCl; pH = 8.5, 3 mM MgCl2),

3 μL template DNA, 1 μL primers (0.5 μL F, 0.5 μL R) (csgA: 0.2 μM) and 8.5 μL sterile DNase/RNase free distilled water, for each target gene. This procedure was done for fimH, mrkD, and foc with the similar protocol. The PCR cycling program was run in accordance with the PCR thermal profile in Table 1.

As aforementioned, the multiplex PCR was employed for the target genes of papG alleles including papGI, papGII and papGIII. Due to this knowledge, The PCR cocktail with a final volume of 25 μL was prepared by adding 12.5 μL Master Mix (2 ×) (Tris- HCl; pH = 8.5, 3 mM MgCl2), 3 μL template DNA, 1 μL primers (0.5 μL F, 0.5 μL R/per each primer) (papGI: 0.2 μM, papGII: 0.2 μM, papGIII: 0.2 μM) and 6.5 μL sterile DNase/RNase free distilled water. The PCR cycling program was done in accordance with Table 4. Next after, the obtained PCR products were run on 1% agarose gel electrophoresis. Ethidium bromide was used as the fluorochrome. The characteristics of genes, fibers and fimbrial subunits are shown in Supplementary Table 1.

Statistical analysis

The obtained results have been described in the format of descriptive statistics in association with the related frequency. Also, the values have been indicated in the form of percentages of the variables [5]. Moreover, the Chi square (χ2) test and Fisher’s exact test were recruited in present study. A P-value of < 0.05 was considered as statistically significant. The statistical analyses were calculated through both of SPSS version 26 software tool and the https://www.icalcu.com/ website.

Results

The age range and the gender of the patients with UTIs

In the current investigation, 108 UPEC strains were isolated from 96 (88.9%) female patients with UTIs and 12 (11.1%) male patients with UTIs. The age range of the patients was between 0 (infants) and 100 years old (Fig. 1).

Fig. 1
figure 1

X- and Y axes show the percentages and the age range of the patients with UTIs, respectively. The highest number of patients (n = 23 (19 females and 4 males) (21.3%)) belongs to the age range of 51–60 while, the lowest one (n = 1 (female) (0.9%)) belongs to the age range of 91–100. The others were 0–10 (n = 8 (7 females and 1 male) (7.4%)), 11–20 (n = 6 (females) (5.6%)), 21–30 (n = 10 (females) (9.3%)), 31–40 (n = 18 (17 females and 1 male) (16.7%)), 41–50 (n = 21 (females) (19.4%)), 61–70 (n = 10 (7 females and 3 males) (9.3%)), 71–80 (n = 9 (7 females and 2 males) (8.3%)) and 81–90 (n = 2 (1 female and 1 male) (1.9%))

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Antimicrobial resistance patterns

The results obtained from AST are shown in Table 2. As Table 2 shows, the first three most influential antibiotics in association with 108 UPEC isolates were nitrofurantoin (93.5%) (with no significant statistical correlation (P > 0.05) between antibiotic susceptibility and gender), chloramphenicol (90.7%) (with no significant statistical correlation (P > 0.05) between antibiotic susceptibility and gender) and gentamicin (88.9%) (with significant statistical correlation (P < 0.05) between antibiotic susceptibility and gender), respectively; while the first three most uninfluential antibiotics were respectively as ampicillin (80.6%) (with no significant statistical correlation (P > 0.05) between antibiotic resistance and gender), fosfomycin (64.8%) (with no significant statistical correlation (P > 0.05) between antibiotic resistance and gender), tetracycline and sulfamethoxazole-trimethoprim (53.7%) (with no significant statistical correlation (P > 0.05) between antibiotic resistance (neither tetracycline nor sulfamethoxazole and trimethoprim) and gender).

Table 2 Results of antibiotic susceptible and non-susceptible UPEC isolates based on Magirakos et al. [29]
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ESBL producing UPEC Isolates

Thirty strains from 108 isolates (27.8%) were detected as ESBL producing UPEC bacterial cells. Four and 26 ESBL producing UPEC strains were isolated from male and female patients, respectively (with no significant statistical correlation (P > 0.05) between ESBL producing UPEC isolates and gender). As Table 3 shows, the first three most influential antibiotics in association with 30 ESBL producing UPEC isolates were chloramphenicol (93.3%), nitrofurantoin (83.3%) and gentamicin (76.7%), respectively; while the first three most uninfluential antibiotics were respectively as amikacin (93.3%), cefotaxime (83.3%) and sulfamethoxazole-trimethoprim (73.3%).

Table 3 Results of antibiotic susceptibility test in association with UPEC producing ESBL isolates based on CLSI 2021 [27]
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Multidrug-resistance (MDR) and extensively drug-resistance (XDR) patterns

The results obtained from AST were screened, rigorously. Seventy-five/108 (69.4%) UPEC strains were identified as MDR strains. Sixty-eight and seven MDR strains were isolated from females and males, respectively. The chi square test shows a significant statistical correlation (P < 0.05) between MDR characteristic and the gender of the UTIs patients. In this regard, 57 different MDR patterns were identified among 75 MDR clinical isolates of UPEC strains (Table 4). The most three predominant MDR patterns were AM-TE-FOS-SXT (8.0%), AM-TE-FOS (7.0%) and AM-TE-SXT (4.0%), respectively. in addition, seven MDR patterns including AM-CTX-CIP-TE-FOS (2.7%), AM-CTX-TE-FOS-SXT (2.7%), AM-CIP-TE-FOS-SXT (2.7%), AM-FEP-CTX-CAZ-CIP-TE-FOS-SXT (2.7%), AM-FEP-CTX-CAZ-CIP-IPM-TE-SXT (2.7%), AM-AN-FEP-CTX-CAZ-CIP-IPM-K-TE-SXT (2.7%) and AM-AN-FEP-CTX-CAZ-C-CIP-IPM-K-TE-FOS (2.7%) ranked fourth. As Table 4 shows, other MDR patterns were unique among the left MDR isolates. In addition to MDR strains, two UPEC isolate (2/108) (1.9%) were recognized as XDR strain (Table 5). No PDR isolate was detected among 108 isolated UPEC strains in the present study.

Table 4 Categorization of Multidrug-resistance (MDR) patterns in UPEC isolates into nine groups and 57 patterns
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Table 5 Extensively drug-resistance (XDR) patterns pertaining to UPEC isolates. The first and second XDR patterns have been recognized in UPEC isolates from patients with UTIs; a male and a female, respectively
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PCR investigation of CU and curli fimbriae genes

In accordance with the obtained results from PCR assay (Supplementary Fig. 1), the highest frequency and distribution of the FAGs belong to fimH (93.3%) (with no significant statistical correlation (P > 0.05) between the frequency of fimH gene and gender) (P < 0.05), csgA (90.4%) (with no significant statistical correlation (P > 0.05) between the frequency of csgA gene and gender) and papG (37.5%) (papGII (30.8%)) (with no significant statistical correlation (P > 0.05) between the frequency of papG gene and gender) (Table 6).

Table 6 Frequency of the FAGs among 104* UPEC isolates
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As four FAG patterns belonging to four UPEC isolates were missed; the left 104 FAGs are presented within the current table (Table 6).

Moreover, 19 different FAG patterns were identified among 104 UPEC strains (Table 7). The most three predominant FAG patterns were.

Table 7 FAG patterns pertaining to UPEC isolates
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csgA-fimH (46.2%), csgA-fimH-papGII (18.3%), and csgA-fimH-foc (6.7%), respectively.

According to the Fisher’s exact test there is no significant statistical correlation (P > 0.05) between the frequency of csgA-fimH, csgA-fimH-papGII, csgA-fimH-foc gene patterns and gender, respectively.

In the current study, several profiles including molecular FAG patterns, phenotypic AMR patterns, ESBL production patterns together with MDR and XDR patterns were provided in accordance with Table 8. As Table 8 indicates, the csgA-fimH FAG pattern encompasses the highest number of phenotypic AMR patterns (36 cases), 30 MDR and 12 ESBL producing strains. According to chi square test, a significant statistical correlation (P < 0.05) between the MDR and ESBL producing UPEC strains can be recognized within the.

Table 8 A full profile of the isolated UPEC strains in the present study
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csgA-fimH FAG pattern. Moreover, an XDR strain has been detected among the isolates bearing the csgA-fimH FAG pattern. The csgA-fimH-papGII FAG pattern includes 16 different phenotypic AMR patterns, 12 MDR isolates and seven ESBL producing strains. The csgA-fimH-foc FAG pattern includes seven different phenotypic AMR patterns, five MDR isolates and two ESBL producing strains. The second XDR strain belongs to the isolate bearing csgA FAG pattern.

Discussion

The genomic plasticity of the bacterial cells of E. coli is significantly high [35]. The bacterial genomic pool or pan-genome is composed of core genome, adaptive (dispensable, flexible, accessory) genome, and singleton genes. The core genome contains housekeeping genes and those genes that are involved in vital activities of the cell [10, 36, 37]. In contrast to core genome, the flexible genome is mostly composed of VGs (virulome) and ARGs (resistome) which play pivotal role in bacterial adaptation [36,37,38]. These genes and the singletons (the unique genes that encode VFs and participate in bacterial pathogenicity) may be acquired through the horizontal genetic transfer (HGT) via the mobile genetic elements (MGE) (mobilome) such as plasmids, transposons, integrons (ints), insertion sequences (ISs), phages, etc. [36,37,38]. Due to this knowledge, the pan-genomic content of E. coli strains ranges from ~ 4.5 Mb (the intestinal commensal strains of E. coli as a population of gut microbiota) to ≥ 5 Mb (the Extraintestinal pathogenic E. coli (ExPEC) like UPEC strains) [9, 12, 37, 39,40,41].

The Gram-negative bacteria of UPEC and K. pneumoniae strains are known as the most important causative bacterial agents of UTIs, respectively [2,3,4, 7, 18, 35, 37]. On the other hand, the rise of AMR feature is a prominent concern, worldwide [42,43,44]. The Gram-negative uropathogens like UPEC encompasses a plastic genome which has a significant potential in association with acquiring a wide range of VGs and ARGs through MGEs via the process of HGT [3, 10, 35, 36, 44, 45]. Due to this knowledge, transmission of antibiotic resistance and virulence factors e.g., bacterial fimbriae can be performed among different strains of UPEC bacterial cells.

In accordance with previous reports, UPEC, K. pneumoniae, uropathogenic Pseudomonas aeruginosa (UPPA), uropathogenic Enterococcus spp., and uropathogenic Enterobacter spp. strains are known as the typical AMR uropathogens that are recognized as the top ten prominent pathogens which may lead to mortality [44, 46]. The rise of production of.

ß-lactamases among UPEC strains is a significant concern; because it leads to increase the number of ESBL producing strains. Resistance to third generation of cephalosporins e.g., ceftazidime and cefotaxime is a clear example in this regard [18, 44]. Sometimes, both of ARGs and VGs are located upon the similar MGEs and this feature may lead to increase the pathogenesis of the uropathogens; however, the genes encoding the studied adhesins in the current survey are normally found on PAIs [36, 44, 47,48,49,50]. In accordance with previous reports, 65% and 75% of the complicated and uncomplicated UTIs and 95% and 50% of the community-acquired UTIs and nosocomial UTIs are respectively, caused by UPEC [42, 51]. The UPEC pathotypes ability in association with bacterial invasion, colonization and biofilm formation in human host urinary system is directly related to fimbriae as adhesion factors [6, 7, 9, 10, 51]. As aforementioned, the high plasticity of UPEC genome and the utilization of HGT to transfer VGs and ARGs in UPEC pathotypes, make this bacterial agent unique to have effective adaptation and rapid evolutionary mechanisms to respond to its own environmental factors including human host immune system biomolecules like interleukins and toll-like receptors and bacterial attachment to specific receptors and bacterial dissemination within human host urinary system [2, 7, 40, 41, 51,52,53,54,55]. The adhesive fimbriae in uropathogens like UPEC are extracellular proteinaceous appendages that support bacterial cells of UPEC to attach to urothelial and bladder cells in human host urinary system. Moreover, these fimbriae empower the attachment of UPEC cells against urine flow. The type 1 fimbriae with a length of 2 μm and a width of 10 nm are located upon the entire surface of UPEC bacterial cells. According to reported results from previous investigations, type 1 fimbriae are detectable in 82% to 100% of the UPEC pathotypes [6, 56,57,58,59]. In the present study, the prevalence of fimH was 93.3%. The FimH as the adhesin subunit of type 1 fimbria is encoded by fimH gene as a part of chromosomal operon of fimBEAICDFGH. Type 1 fimbriae are attached to uroplakins and their expression can be switch on or switch off via the environmental factors [6].

Type 3 fimbria is another member of CUF that has pivotal role in UPEC strains colonization and biofilm formation. These CU fibers have a length of 0.5–2 μm and a width of 2–4 nm [6, 9, 10, 18]. The mrkABCDF operon in UPEC pathotypes originates from K. pneumoniae which normally are transferred via HGT. The mrk operons are located on different positions e.g., transposon, conjugative plasmid or chromosome [6, 18,19,20, 60]. MrkD is the adhesin subunit of type 3 fibers. The presence of mrkD gene in UPEC strains varies from 2% (isolated from patients with non-CAUTIs) to 93.3% (isolated from patients with CAUTIs [18, 61]. In present study, the prevalence of mrkD gene (type 3 fimbriae) was 2.9%.

F1C fimbriae are encoded by the chromosomal operon of focAICDFGH. In accordance with previous studies, a close homology has been recognized between F1C and type 1 fimbriae. FocG is the minor subunit and FocH acts as adhesin. These proteins are encoded by the focG and focH genes. F1C fibers are involved in different types of UTIs via contribution to sticky bacterial colonization and biofilm formation which support the UPEC bacterial cells against urine flow. F1C fibers have high activities in the absence of type 1 and P fimbriae. Normally, they have 1 μm length and 7 nm width [6, 9, 10]. The prevalence of F1C fibers varies from 0 to 30% [6, 57, 62]. Indeed, there are cross-talks between fimbrial structures of F1C fimbriae, type 1fimbriae, P fimbriae and bacterial motility structures of flagella. By the UPEC strains colonization, the expression of those genes that encode flagellar subunits get reduced [16, 63,64,65]. In the present study, the prevalence of focGH genes was 20.2%.

P fimbriae are encoded by the operon of papIBAHCDJKEFG which are located on pathogenicity islands (PAIs). PapG as the tip adhesin of P fiber is encoded by three alleles of papGI, papGII and papGIII for the most [6, 10, 51]. Although the allele gene of papGIV has been detected, its prevalence and function has not been described, in details [11, 24, 51]. PapGII class has been recognized as the most frequent adhesin among UPEC strains. The P fimbriae contribute in upper UTIs for the most [6, 10, 51]. In an investigation, the prevalence of PapG among UPEC isolates was reported as 23.2% (PapGIII > PapGII > PapGI) [66]. As the reported results from previous studies show, the prevalence of papG operon varies from 5–7% among commensal isolates of E. coli to 14%-28% and 71%-91% in UPEC strains isolated from patients with cystitis and pyelonephritis, respectively [51, 67]. In a recent survey, the prevalence of papGII and papGIII genes in isolated UPEC strains from patients with pyelonephritis and cystitis relating to UTI was 68% and 31%, respectively; while, the prevalence of papGI and papGIV genes in isolated UPEC strains from patients with cystitis relating to UTI was only 1% (PapGII > PapGIII > PapGI and PapGIV) [11]. In our study, the prevalence of papG, papGI, papGII and papGIII genes was identified as 37.5%, 2.9%, 30.8% and 3.8% (PapGII > PapGIII > PapGI), respectively.

Curli fibers are known as effective functional amyloids which significantly contribute to bacterial biofilm formation and development [68, 69]. The extracellular and superficial proteaceous curli fibers have similar structural and biochemical characteristics with eukaryotic amyloid fibers. The presence of these straight and unbranched curli fibers which are enriched by ß-sheet structures is related to important diseases e.g., Alzheimer's and Parkinson's diseases in humans [68,69,70,71,72]. The CsgA protein is the major curli subunit which have effective role in curli fibers polymerization upon the bacterial cell surface [51]. In one study, the prevalence of csgA gene among UPEC strains isolated from patients with UTI (cystitis) was reported as 100% [68], while in another study, the prevalence of csgA gene among UPEC strains isolated from patients with UTI was reported as 30% [67]. In the present investigation, the prevalence of the csgA gene was 90.4% (P < 0.05).

In our study, we were able to represent 19 different FAG patterns in association with the isolated UPEC strains. One of the isolates had no related genes at all. Although the prevalence of the FAG pattern relating to fimH and csgA genes was respectively 2.9% and 3.8%, the FAG pattern belonging to csgA-fimH with the prevalence of 46.2% ranks first among 19 different FAG patterns. The second and third FAG patterns belong to.

csgA-fimH-GII (18.3%) and csgA-fimH-foc (6.7%).

Moreover, we have obtained interesting results in association with phenotypic AMR patterns, phenotypic ESBL, MDR and XDR strains among isolated UPEC in present study (Tables 2, 3, 4 and 5). As we know, the AMR feature ranks as the top ten threats in association with public health, worldwide [43]. Therefore, it is recommended to administer and use antibiotics only regarding to symptomatic UTIs [73]. Moreover, there are thousands of studies that present different antibiotic resistance patterns in isolated microbial uropathogens including UPEC, worldwide. There are several global guidelines which are published during certain intervals including European Association of Urology (https://uroweb.org/) and Clinical and Laboratory Standards Institute (CLSI) (https://clsi.org/) in association with the use of antibiotics.

In recent years, our major concern is about of the increase of the MDR, XDR and PDR pathogens which are appeared through the prolonged use of antibiotics for treating different types of infectious diseases e.g., UTIs. By the increase of global drug resistance pathogens, the cost of treatments rises up. Due to this knowledge, significant number of scientists are trying to develop new strategies regarding the non-antibiotic therapeutic alternatives [74]. In this regard several strategies including the use of probiotics, microbiota transplantation, nanoparticles, phage therapy, nutraceuticals, herbal medicine, immunomodulant compounds, vaccination and anti-adhesive therapeutics have been suggested [39, 42, 74,75,76]. The authors believe that recruitment of anti-adhesive therapeutics can be an effective choice in this regard; because, fimbriae are the main weapons that initiate bacterial adherence that may lead to bacterial invasion, colonization, biofilm formation and AMR feature. Neutralization of these effective fimbrial adhesins leads to ejection of bacterial pathogens like UPEC from the human host body without any attachment. Moreover, these fimbrial adhesins are common among a wide range of uropathogens. Due to this knowledge, the feature of microbial drug resistance will be neutralized by the time. So, working on effective anti-adhesive agonists and antagonists against important and pivotal fimbrial adhesins including curli fibers, type 1 and P fimbriae is worthy to reduce the rate of UTIs, infectious morbidity and mortality, cost of public health systems and drug resistance feature.

Conclusions

In conclusion, detection, providing and designing of patterns and profiles in association with FAGs, AMR feature in UPEC strains give us an effective option to have a successful and influential prevention for both of UTIs initiation and AMR feature.

Limitations of the study

In some cases, we missed the data in association with bacterial genes and phenotypic antibiotic resistance profiles which have been mentioned within the tables.

Strength of the study

Fortunately, we were able to provide 19 effective FAG patterns, a versatile of phenotypic resistance patterns, 57 MDR patterns and two XDR pattern in association with clinical isolates of UPEC strains to provide influential data and information through tables from Tehran, the Capital city of Iran.

Availability of data and materials

The datasets used and/or analysed during the current study available from the corresponding author on reasonable request.

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Acknowledgements

We have special thanks to Cyrus Chegini (the research laboratory expert, college of basic sciences, Shahr-e-Qods branch, Islamic Azad University, Tehran, Iran), Ali Samadi, Mohammad Hossein Heydargoy, Reza Seifollahi, Amir Cheraghi, Samira Alizad Paydar, Yasaman Bahramvand, Hasan Mohammadnezhad Pahmedani for their sincere full support and kind help in this investigation.

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  1. Department of Microbiology, Shahr-E-Qods Branch, Islamic Azad University, Tehran, 37541-374, Iran

    Taha Golpasand, Mohammad Keshvari & Payam Behzadi

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Contributions

Conceptualization: P.B.; Methodology: P.B.; Software: P.B., T.G., M.K.; Statistical Analysis: P.B., T.G.; Validation: P.B., T.G., M.K.; Formal analysis: P.B., T.G., M.K.; Investigation: P.B., T.G., M.K.; Resources: P.B., T.G., M.K.; Data curation: P.B., T.G., M.K.; Writing—Original Draft preparation: P.B., T.G., M.K.; Writing—Review and Editing: P.B.; Visualization: P.B., T.G.; Supervision: P.B.; Project administration: P.B.; Research assistant: T.G.; Team Leadership: P.B.; Funding acquisition: None; Financial Sponsorship: P.B.; All authors have read and agreed to the published version of the manuscript.”

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Correspondence to Payam Behzadi.

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This scientific investigation has been performed under the permission number of DP/97/220 (97/12/12), issued by the Research Council of the Islamic Azad University, Shahr-e-Qods Branch. Since, the urine samples and the related information in association with the patients with UTIs were enrolled by the Labs’ and hospital’s technicians and experts and all these materials were anonymous to the authors, no ethical approval was needed for this project. This study was achieved according to the Declaration of Helsinki guidelines.

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Payam BEHZADI is the BMC Microbiology Editorial Board Member.

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Golpasand, T., Keshvari, M. & Behzadi, P. Distribution of chaperone-usher fimbriae and curli fimbriae among uropathogenic Escherichia coli. BMC Microbiol 24, 344 (2024). https://doi.org/10.1186/s12866-024-03472-5

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