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1 Microbial Adhesion Group, Centre for Biomedical Microbiology, BioCentrum-DTU, Technical University of Denmark, DK-2800 Lyngby, Denmark
2 School of Molecular and Microbial Sciences, University of Queensland, Brisbane, QLD 4072, Australia
Correspondence
Per Klemm
pkl{at}biocentrum.dtu.dk
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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The GenBank/EMBL/DDBJ accession number for the E. coli strain 83972 foc gene cluster is DQ301498.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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). Acute pyelonephritis and asymptomatic bacteriuria (ABU) represent the two extremes of UTI. Acute pyelonephritis is a severe acute systemic infection caused by uropathogenic Escherichia coli (UPEC) clones with virulence genes clustered on ‘pathogenicity islands' (Eden et al., 1976; Funfstuck et al., 1986; Johnson, 1991; Orskov et al., 1988; Stenqvist et al., 1987; Welch et al., 2002). ABU, on the other hand, is an asymptomatic carrier state that resembles commensalism. ABU patients may carry >105 c.f.u. ml–1 of a single E. coli strain for months or years without provoking a host response. In early studies this was explained by a lack of virulence genes, as the majority of ABU-associated E. coli strains are non-haemolytic, non-adherent and lack haemagglutination ability (Eden et al., 1976; Kaijser & Ahlstedt, 1977; Lindberg et al., 1975). Molecular epidemiology has shown, however, that >60 % of ABU strains carry virulence genes even though they fail to express the phenotype (Plos et al., 1990, 1995).
The ability of UPEC to cause symptomatic UTI is enhanced by adhesins, e.g. F1C, P and type 1 fimbriae (Klemm & Schembri, 2000; Oelschlaeger et al., 2002). Tissue surfaces in the urinary tract are submitted to strong hydrodynamic shear forces. Adherence to the urinary tract epithelium enables the bacteria to resist the hydrodynamic forces of urine flow and to establish infection. F1C fimbriae are expressed by a large proportion of urinary tract infectious E. coli strains; depending on the study 14–30 % of UTI strains have been reported to be able to express these fimbriae (Pere et al., 1987; Siitonen et al., 1993). F1C fimbriae, like P and type 1 fimbriae, are surface polymers 7 nm wide and approximately 1 µm long. The bulk of an F1C fimbria is made up of about 1000 subunits of a major building element, the FocA protein. Additionally, a few copies of minor components, FocF, FocG and FocH, are integral parts of the fimbria, and are responsible for its adhesive properties. Export of the structural components of the fimbriae to the surface depends on a periplasmic chaperone, FocC, and an outer-membrane-located usher, FocD (Klemm et al., 1994, 1995). F1C fimbriae specifically recognize galatosylceramide targets present on epithelial cells in the kidneys, ureters and bladder as well as globotriaosylceramide, present only in the kidneys (Bäckhed et al., 2002; Khan et al., 2000). Recently, it was shown that human renal epithelial cells specifically produce the proinflammatory cytokine IL-8 in response to F1C-mediated attachment (Bäckhed et al., 2002).
The ABU strain E. coli 83972 is a clinical isolate capable of long-term bladder colonization. The strain was originally isolated from a young Swedish girl with ABU who had carried it for at least 3 years without symptoms (Andersson et al., 1991; Lindberg et al., 1975). It is well adapted for growth in the urinary tract, where it establishes long-term bacteriuria (Andersson et al., 1991; Hull et al., 2000; Wullt et al., 1998, 2000). The strain has successfully been used for prophylactic purposes in patients with recurrent UTI. Here the bladders of patients are deliberately colonized with strain 83972 in order to prevent the establishment of UPEC stains. The ability of E. coli 83972 to establish efficient long-term colonization of the human bladder without evoking countermeasures from the host defences is not fully understood. The strain has been reported to carry genes of the pap, fim and foc gene clusters, encoding P, type 1 and F1C fimbriae, respectively (Hull et al., 1999). We have recently demonstrated that the strain is unable to express functional P and type 1 fimbriae (Klemm et al., 2006). In this study we investigate the status of the foc genes and corresponding F1C fimbriae in this interesting strain.
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METHODS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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. E. coli 83972 is a prototype ABU strain and lacks defined O and K surface antigens. It carries adhesin gene clusters homologous to fim, pap and foc but does not seem to express functional fimbrial adhesins after in vitro culture or when recovered from the urinary tract (Andersson et al., 1991; Hull et al., 1999). The 83972 pap : : kan mutant was constructed using the 
Red recombinase gene replacement system (Datsenko & Wanner, 2000). Briefly, the npt gene from plasmid pKD4 was amplified by primers containing 50-nucleotide pap homology extensions (papf, 5'-CAGGGCCAGGGAGAAGTAACTTTCAAAGGAACTGTTGTTGACGCTCCATGGTGTAGGCTGGAGCTGCTTC-3' and papr, 5'-CCTTTGTCCACGCCATTAACCGAAACAATGGAGTCCCAGCCATGACCCAGCATATGAATATCCTCCTTA-3'). This product was digested with DpnI and transformed into 83972(pKD46), and kanamycin-resistant colonies were selected. The Red helper plasmid pKD46 was cured by growth at 37 °C and the correct double-crossover and recombination event was confirmed by PCR and DNA sequencing. This strain, designated 83972pap, therefore contains a deletion in the region spanning the papA-papG genes. Cells were routinely grown at 37 °C on solid or in liquid Luria–Bertani (LB) medium supplemented with the appropriate antibiotics unless otherwise stated.
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Agglutination assays.
The capacity of bacteria to express hybrid F1C fimbriae with incorporated FimH was assayed by their ability to agglutinate yeast (Saccharomyces cerevisiae) cells on glass slides. Aliquots of washed bacterial suspensions at OD600 0.5 and 5 % yeast cells were mixed and the time until agglutination occurred was measured.
Western immunoblotting.
For maximized expression of F1C fimbriae, cells were grown in 100 ml filter-sterilized pooled human urine. Fimbrial proteins detached from the surface of the cells by blending and proteins from total cell lysates were separated on 15 % polyacrylamide gels by SDS-PAGE. The proteins were then transferred to PVDF membranes. The membranes were blocked with 0.5 % Tween-20 and incubated with anti-F1C fimbriae serum, which was a generous gift from Timo Korhonen (University of Helsinki, Finland) and Ulrich Dobrindt (University of Würzburg, Germany). The membrane was then incubated with horseradish-peroxidase-labelled antibodies followed by visualization with tetramethylbenzidine (TMB).
Microarray analysis.
The microarray results of the foc cluster are extracted from a previously published complete genome microarray study of E. coli 83972; the experimental design, data analysis and verification of the microarray results have been described (Roos et al., 2006). In short, mid-exponential cultures of strain 83972 grown in pooled human urine or MOPS minimal medium supplemented with 0.2 % glucose were used for inoculation of 50 ml urine or MOPS to an OD600 of 0.05 and 5 ml samples for isolation of RNA were extracted from three individual cultures at mid-exponential phase. The cultures were grown at 37 °C and 130 r.p.m. Extracted samples were immediately mixed with 2 vols RNAprotect Bacteria Reagent (Qiagen), and incubated for 5 min at room temperature to stabilize RNA. Total RNA was isolated using the RNeasy Mini kit (Qiagen), and eluted RNA samples were treated with DNase I and repurified using RNeasy Mini Columns. The quality of the total RNA was examined by agarose gel electrophoresis and by measuring the absorbance at 260 and 280 nm. Conversion of RNA to cDNA, hybridization, washing and staining were performed according to the GeneChip Expression Analysis Technical Manual 701023 Rev. 4 (Affymetrix) and the microarrays were scanned using the GeneChip Scanner 3000. GeneChip E. coli Genome 2.0 Arrays (Affymetrix) were used for hybridization of the labelled cDNA. Three chips were hybridized with samples from E. coli 83972 grown in MOPS in triplicate and three chips were hybridized with cells grown in pooled human urine in three individual flasks. The GeneChip E. coli Genome 2.0 Array includes approximately 10 000 probe sets for all 20 366 genes present in the K-12 (MG1655), CFT073 (uropathogenic), O157 : H7-EDL933 (enterohaemorrhagic) and O157 : H7-Sakai (enterohaemorrhagic) genomes. Array normalization and expression value calculation were performed using the DNA-Chip Analyzer (dChip) 1.3 software program (http://www.dchip.org/) (Li & Wong, 2001). The three arrays hybridized with samples from E. coli 83972 grown in MOPS were used as the baseline for calculation of fold changes on the three arrays hybridized with samples from E. coli 83972 grown in urine.
Verification of microarray results.
RT-PCR was performed to confirm DNA microarray gene expression data. Total RNA was isolated exactly as described above and treated with DNase I to remove any traces of DNA. RNA was converted to cDNA using SuperScript II (Invitrogen Life Technologies). cDNA was used directly as template for PCR and a negative control on the RNA sample (not converted to cDNA) was run in parallel to confirm that all DNA had been removed in the earlier step. The total number of cycles used in PCR ranged from 12 to 30. RT-PCR was performed to verify the transcript levels for an example gene, papA. The following primers were used in RT-PCR and PCR: papA, 620 (5'-GTGAAGTTTGATGGGGCGACC-3') and 621 (5'-CGCAACTGCTGAGAAAGCACC-3'); 16S, 622 (5'-CGGATTGGAGTCTGCAACTCG-3') and 623 (5'-CACAAAGTGGTAAGCGCCCTC-3'). papA was significantly up-regulated 19-fold in urine and showed very low signals in MOPS. papA could not be detected in the samples from MOPS, not even after 30 cycles of PCR, while papA was detected in all three urine samples, visualized as strong bands on an agarose gel. 16S was used as a normalizing internal standard and was detected with the same intensity in all samples.
Transmission electron microscopy.
Cells were prepared from freshly grown colonies on LB agar and resuspended in a drop of sterile ultrapure water. A glow-discharged Formvar-coated copper grid was placed on to the drop for approximately 1 min to allow the cells to adsorb. Excess liquid was removed from the grid with a piece of filter paper before a drop of 1 % ammonium molybdate (negative stain) was placed on the grid. After a few seconds the grid was blotted dry and the preparation was observed under a JEOL JEM1010 transmission electron microscope operated at 80 kV. The images were captured using an analySIS Megaview III digital camera.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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). focA showed a high expression level in MOPS and was significantly up-regulated 1.8-fold in urine, displaying the 21st highest signal in urine out of a total of 8716 transcripts. Also the sfaB and focI genes showed significant up-regulation: 2.7- and 2.4-fold, respectively. Taking these results together it seems that growth in urine up-regulates the expression of genes in the foc gene cluster. Arguably, expression of F1C fimbriae might be implicated in the ability of strain 83972 to colonize the human bladder.
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). This indicated that strain 83972 did not produce F1C fimbriae or that these organelles were present in very low numbers.
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). Since F1C and P fimbriae are morphologically identical, the pap genes, responsible for P fimbriae production, were deleted from the genome of strain 83972, resulting in strain 83972pap. Electron microscopy of 83972pap revealed that it is completely bald, showing no indication of either expression of F1C or any other fimbriae (Fig. 3a). Meanwhile, we proceeded to probe for the presence of FocA protein in total cell lysates of strain 83972. Indeed it turned out that although the strain did not express F1C fimbriae, small amounts of the major building element of the fimbriae, FocA, could be detected but this was apparently not assembled into fimbriae (Fig. 2
).
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, 1995). For example the mannose-binding FimH adhesin of type 1 fimbriae can be displayed as an integral component of F1C fimbriae, giving rise to bacterial hosts capable of yeast agglutination (Klemm et al., 1994). This feature can be employed to monitor expression of F1C fimbriae in strain 83972 because, although the fim gene cluster in the strain has a large deletion, the fimH gene is intact, expressed, and gives rise to a functional adhesin (Klemm et al., 2006). When a plasmid, pPKL143, containing the intact foc gene cluster was transformed into strain 83972pap the resulting cells readily agglutinated yeast cells, indicative of surface-exposed F1C hybrid fimbriae (with integrated FimH).
To probe the foc gene cluster of strain 83972 for non-functional genes the strain was transformed with plasmids harbouring various foc genes and the resultant transformants were tested for their ability to agglutinate yeast cells (Table 2). Only one of these, transformed with plasmid pPKL160 encoding the focCD sector, showed positive yeast agglutination. Transformants containing a cut-down version of this plasmid (pPKL332), encoding only an intact focD gene, were also positive. Furthermore, fimbriae purified from the surface of 83972 cells harbouring plasmid pPKL332 reacted positively with FocA antisera in Western blotting experiments (Fig. 2). To confirm the expression of F1C fimbriae we examined the different strains by transmission electron microscopy. In contrast to cells of 83972pap, which were completely bald, 83972pap cells harbouring pPKL332 (focD) were highly fimbriated (Fig. 3).
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). No deletions or premature stop codons were identified and the analysis revealed that all predicted open reading frames are maintained. Sequence divergence was observed for the major structural subunit-encoding gene focA (one base substitution) and the minor subunit-encoding gene focF (two base substitutions), resulting in 100 % and 98 % amino acid identity for FocA and FocF, respectively. FocF contained the two amino acid substitutions L52F and S88R as compared with CFT073. However, FocF from strain 83972 shows 99 % amino acid identity with SfaG, an S-fimbrial adhesin protein, from the uropathogenic strain 536, and the two amino acid residues in positions 52 and 88 are identical to those of SfaG in 536. Strain 536 is known to express functional S fimbriae (Ott et al., 1988), indicating that the two amino acid substitutions in FocF of the 83972 relative CFT073 might not be crucial for the functionality of this subunit, which is in agreement with our yeast agglutination results (Table 2).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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, 1995, 2004). Finally, the strain has a copy of the F14 papA variant that has been associated with other virulence factors, including S and F1C fimbriae, haemolysin and cytotoxic necrotizing factor 1 from E. coli strains in the phylogenetic group B2 (Johnson et al., 2001).
In this work we found that expression of the foc genes was significantly up-regulated in strain 83972 by exposure to and growth in human urine. Meanwhile, when we defined the molecular status of F1C fimbriae we found that this important fimbrial adhesin cannot be expressed due to a defunct transport system. This finding underlines the importance of F1C fimbriae in urinary tract colonization. Arguably, the ancestor of strain 83972 was once able to express F1C, type 1 and P fimbriae, all of which are associated with UPEC strains. It is interesting to note that all of these fimbriae have been demonstrated to trigger aggressive host defence mechanisms such as production of cytokines, inflammation and exfoliation of infected epithelial cells (Bäckhed et al., 2002; Hedlund et al., 2001; Mulvey et al., 1998; Samuelsson et al., 2004; Wullt et al., 2003). It seems feasible that the failure of strain 83972 to trigger symptoms in a human host can to a large degree be accounted for by its inability to express functional F1C, type 1 and P fimbriae. Interestingly, it was recently found that in the UPEC strain CFT073 the loss of P and type 1 fimbriae appears to be compensated for by expression of F1C fimbriae (Snyder et al., 2005). Obviously strain 83972 cannot do this because here all three systems are defunct. Also, the non-functional FocD cannot be complemented by other fimbrial ushers because the fimD gene is truncated (Klemm et al., 2006) and complementation with the PapC usher does not work (our unpublished results). In contrast to organisms that have acquired genes for pathogenesis, E. coli 83972 is an example of an organism that has adapted to commensalism through gene loss and mutations. The relationship between bacterium and host in a persistent infection is a mutual trade off. In this case the bacterium has lost its primary colonization factors; however, having done so it does not damage the host and evades immune surveillance. In effect the strain has become domesticated to a degree where it does not cause any symptoms: it has become benign.
According to the literature, E. coli 83972 was carried by a young girl for 3 years without any symptoms. Whether the strain had already lost the ability to express F1C fimbriae previously during passage in another host or did so in this particular girl is unclear. If gene functions are directly detrimental due to conditions in the environment then mutations will be selected for which render them non-functional. In E. coli 83972 the F1C system is probably inactivated by adaptive mutations as a trade-off with the host. Genes of non-functional products tend to erode over time through accumulation of mutations. There are many instances where genome shrinkage has been associated with bacterial lifestyle transition (Moran, 2002). It is interesting to note that the type 1, P and F1C fimbrial systems of E. coli 83972 have been incapacitated in quite different ways: the type 1 system by a major deletion encompassing 4.5 kb of the fim gene cluster and P fimbriae by point mutations in the papG gene rendering the PapG adhesin non-functional. Finally, the F1C system has been inactivated by point mutations in the fimbrial transport system. The Q472L mutation is the likely candidate for inactivation of FocD since it is highly conserved among fimbrial ushers. Arguably, this residue plays a role in the function and/or stability of the protein. However, the foc genes are still transcribed and the major structural protein, FocA, is produced although it is unable to reach the cell surface. This suggests that the inactivation of FocD is a recent evolutionary event.
Recently, we found that strain 83972 grows extremely well in human urine (Roos et al., 2006). It might well be that these excellent growth characteristics account for its faculty for long-term bladder colonization. Strain 83972 has been used in several human inoculation studies and plays a key role in the success of this protocol by establishing bacteriuria without jeopardizing the health of the patient (Wullt et al., 1998, 2000; Wullt, 2003). Deliberate colonization with E. coli 83972 has been shown to reduce the frequency of UTI in patients with neurogenic bladder secondary to spinal cord injury (Hull et al., 2000) and the strain can prevent catheter colonization by bacterial and fungal uropathogens (Darouiche et al., 2001; Trautner et al., 2002, 2003). This study sheds new light on how E. coli 83972 has adapted to grow in the human bladder. The strain has lost the ability to express functional F1C, type 1 and P fimbriae and thus is able to persist in this environment without triggering a host immune response.
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ACKNOWLEDGEMENTS |
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Received 23 November 2005;
revised 13 February 2006;
accepted 22 February 2006.
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 S.-P. Nuccio and A. J. Baumler Evolution of the Chaperone/Usher Assembly Pathway: Fimbrial Classification Goes Greek Microbiol. Mol. Biol. Rev., December 1, 2007; 71(4): 551 - 575. [Abstract] [Full Text] [PDF]
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A. T. Anfora, B. J. Haugen, P. Roesch, P. Redford, and R. A. Welch Roles of Serine Accumulation and Catabolism in the Colonization of the Murine Urinary Tract by Escherichia coli CFT073 Infect. Immun., November 1, 2007; 75(11): 5298 - 5304. [Abstract] [Full Text] [PDF]
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P. Klemm, V. Hancock, and M. A. Schembri Mellowing Out: Adaptation to Commensalism by Escherichia coli Asymptomatic Bacteriuria Strain 83972 Infect. Immun., August 1, 2007; 75(8): 3688 - 3695. [Full Text] [PDF]
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V. Hancock and P. Klemm Global Gene Expression Profiling of Asymptomatic Bacteriuria Escherichia coli during Biofilm Growth in Human Urine Infect. Immun., February 1, 2007; 75(2): 966 - 976. [Abstract] [Full Text] [PDF]
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 A. T. Anfora and R. A. Welch DsdX Is the Second D-Serine Transporter in Uropathogenic Escherichia coli Clinical Isolate CFT073. J. Bacteriol., September 1, 2006; 188(18): 6622 - 6628. [Abstract] [Full Text] [PDF]
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fim(pPKL163, all foc genes except focD); lane 2, surface proteins of E. coli 83972pap; lane 3, total cell proteins of E. coli 83972pap; lane 4, surface proteins of E. coli 83972pap(pPKL332, focD+); lane 5, surface proteins of E. coli 83972pap(pPKL143, all foc genes).