The mat (or ecp) fimbrial operon is ubiquitous and conserved in Escherichia coli, but its functions remain poorly described. In routine growth media newborn meningitis isolates of E. coli express the meningitis-associated and temperature-regulated (Mat) fimbria, also termed E. coli common pilus (ECP), at 20 °C, and here we show that the six-gene (matABCDEF)-encoded Mat fimbria is needed for temperature-dependent biofilm formation on abiotic surfaces. The matBCDEF deletion mutant of meningitis E. coli IHE 3034 was defective in an early stage of biofilm development and consequently unable to establish a detectable biofilm, contrasting with IHE 3034 derivatives deleted for flagella, type 1 fimbriae or S-fimbriae, which retained the wild-type biofilm phenotype. Furthermore, induced production of Mat fimbriae from expression plasmids enabled biofilm-deficient E. coli K-12 cells to form biofilm at 20 °C. No biofilm was detected with IHE 3034 or MG1655 strains grown at 37 °C. The surface expression of Mat fimbriae and the frequency of Mat-positive cells in the IHE 3034 population from 20 °C were high and remained unaltered during the transition from planktonic to biofilm growth and within the matured biofilm community. Considering the prevalence of the highly conserved mat locus in E. coli genomes, we hypothesize that Mat fimbria-mediated biofilm formation is an ancestral characteristic of E. coli.
BlackburnD.,
HusbandA.,
SaldañaZ.,
NadaR. A.,
KlenaJ.,
QadriF.,
GirónJ. A.2009; Distribution of the Escherichia coli common pilus among diverse strains of human enterotoxigenic E. coli. J Clin Microbiol 47:1781–1784
BlattnerF. R.,
PlunkettG.III,
BlochC. A.,
PernaN. T.,
BurlandV.,
RileyM.,
Collado-VidesJ.,
GlasnerJ. D.,
RodeC. K. & other authors; 1997; The complete genome sequence of Escherichia coli K-12. Science 277:1453–1462
de ReeJ. M.,
SchwillensP.,
van den BoschJ. F.1986; Monoclonal antibodies for serotyping the P fimbriae of uropathogenic Escherichia coli. J Clin Microbiol 24:121–125
DonnenbergM. S.,
KaperJ. B.1991; Construction of an eae deletion mutant of enteropathogenic Escherichia coli by using a positive-selection suicide vector. Infect Immun 59:4310–4317
GenevauxP.,
MullerS.,
BaudaP.1996; A rapid screening procedure to identify mini-Tn 10 insertion mutants of Escherichia coli K-12 with altered adhesion properties. FEMS Microbiol Lett 142:27–30
HammarM.,
ArnqvistA.,
BianZ.,
OlsénA.,
NormarkS.1995; Expression of two csg operons is required for production of fibronectin- and congo red-binding curli polymers in Escherichia coli K-12. Mol Microbiol 18:661–670
HancockV.,
KlemmP.2007; Global gene expression profiling of asymptomatic bacteriuria Escherichia coli during biofilm growth in human urine. Infect Immun 75:966–976
LasaroM. A.,
SalingerN.,
ZhangJ.,
WangY.,
ZhongZ.,
GoulianM.,
ZhuJ.2009; F1C fimbriae play an important role in biofilm formation and intestinal colonization by the Escherichia coli commensal strain Nissle 1917. Appl Environ Microbiol 75:246–251
MacfarlaneS.,
MacfarlaneG. T.2006; Composition and metabolic activities of bacterial biofilms colonizing food residues in the human gut. Appl Environ Microbiol 72:6204–6211
MillerV. L.,
MekalanosJ. J.1988; A novel suicide vector and its use in construction of insertion mutations: osmoregulation of outer membrane proteins and virulence determinants in Vibrio cholerae requires toxR. J Bacteriol 170:2575–2583
MobleyH. L.,
JarvisK. G.,
ElwoodJ. P.,
WhittleD. I.,
LockatellC. V.,
RussellR. G.,
JohnsonD. E.,
DonnenbergM. S.,
WarrenJ. W.1993; Isogenic P-fimbrial deletion mutants of pyelonephritogenic Escherichia coli: the role of αGal(1–4) βGal binding in virulence of a wild-type strain. Mol Microbiol 10:143–155
NowrouzianF. L.,
WoldA. E.,
AdlerberthI.2005; Escherichia coli strains belonging to phylogenetic group B2 have superior capacity to persist in the intestinal microflora of infants. J Infect Dis 191:1078–1083
Obata-YasuokaM.,
Ba-TheinW.,
TsukamotoT.,
YoshikawaH.,
HayashiH.2002; Vaginal Escherichia coli share common virulence factor profiles, serotypes and phylogeny with other extraintestinal E. coli. Microbiology 148:2745–2752
O'TooleG. A.,
KolterR.1998; Initiation of biofilm formation in Pseudomonas fluorescens WCS365 proceeds via multiple, convergent signalling pathways: a genetic analysis. Mol Microbiol 28:449–461
PalestrantD.,
HolzknechtZ. E.,
CollinsB. H.,
ParkerW.,
MillerS. E.,
BollingerR. R.2004; Microbial biofilms in the gut: visualization by electron microscopy and by acridine orange staining. Ultrastruct Pathol 28:23–27
PardeeA. B.,
JacobF.,
MonodJ.1959; The genetic control and cytoplasmic expression of “inducibility” in the synthesis of β-galactosidase by E. coli. J Mol Biol 1:165–178
PicardB.,
GarciaJ. S.,
GouriouS.,
DuriezP.,
BrahimiN.,
BingenE.,
ElionJ.,
DenamurE.1999; The link between phylogeny and virulence in Escherichia coli extraintestinal infection. Infect Immun 67:546–553
PouttuR.,
PuustinenT.,
VirkolaR.,
HackerJ.,
KlemmP.,
KorhonenT. K.1999; Amino acid residue ala-62 in the FimH fimbrial adhesin is critical for the adhesiveness of meningitis-associated Escherichia coli to collagens. Mol Microbiol 31:1747–1757
PrattL. A.,
KolterR.1998; Genetic analysis of Escherichia coli biofilm formation: roles of flagella, motility, chemotaxis and type I pili. Mol Microbiol 30:285–293
ReisnerA.,
HaagensenJ. A.,
SchembriM. A.,
ZechnerE. L.,
MolinS.2003; Development and maturation of Escherichia coli K-12 biofilms. Mol Microbiol 48:933–946
RendónM. A.,
SaldañaZ.,
ErdemA. L.,
Monteiro-NetoV.,
VázquezA.,
KaperJ. B.,
PuenteJ. L.,
GirónJ. A.2007; Commensal and pathogenic Escherichia coli use a common pilus adherence factor for epithelial cell colonization. Proc Natl Acad Sci U S A 104:10637–10642
RhenM.,
KnowlesJ.,
PenttiläM. E.,
SarvasM.,
KorhonenT. K.1983; P fimbriae of Escherichia coli: molecular cloning of DNA fragments containing the structural genes. FEMS Microbiol Lett 19:119–123
RömlingU.,
BianZ.,
HammarM.,
SierraltaW. D.,
NormarkS.1998; Curli fibers are highly conserved between Salmonella typhimurium and Escherichia coli with respect to operon structure and regulation. J Bacteriol 180:722–731
RosenD. A.,
HootonT. M.,
StammW. E.,
HumphreyP. A.,
HultgrenS. J.2007; Detection of intracellular bacterial communities in human urinary tract infection. PLoS Med 4:e329
RussoT. A.,
JohnsonJ. R.2000; Proposal for a new inclusive designation for extraintestinal pathogenic isolates of Escherichia coli: ExPEC. J Infect Dis 181:1753–1754
SaldañaZ.,
ErdemA. L.,
SchüllerS.,
OkekeI. N.,
LucasM.,
SivananthanA.,
PhillipsA. D.,
KaperJ. B.,
PuenteJ. L.,
GirónJ. A.2009; The Escherichia coli common pilus and the bundle-forming pilus act in concert during the formation of localized adherence by enteropathogenic E. coli. J Bacteriol 191:3451–3461
SchembriM. A.,
KlemmP.2001; Biofilm formation in a hydrodynamic environment by novel FimH variants and ramifications for virulence. Infect Immun 69:1322–1328
SelanderR. K.,
KorhonenT. K.,
Väisanen-RhenV.,
WilliamsP. H.,
PattisonP. E.,
CaugantD. A.1986; Genetic relationships and clonal structure of strains of Escherichia coli causing neonatal septicemia and meningitis. Infect Immun 52:213–222
SiitonenA.1992; Escherichia coli in fecal flora of healthy adults: serotypes, P and type 1C fimbriae, non-P mannose-resistant adhesins, and hemolytic activity. J Infect Dis 166:1058–1065
SimonR.,
PrieferU.,
PühlerA.1983; A broad host range mobilization system for in vivo genetic engineering: transposon mutagenesis in gram-negative bacteria. Biotechnology 1:784–791
SokurenkoE. V.,
CourtneyH. S.,
MaslowJ.,
SiitonenA.,
HastyD. L.1995; Quantitative differences in adhesiveness of type 1 fimbriated Escherichia coli due to structural differences in fimH genes. J Bacteriol 177:3680–3686
SokurenkoE. V.,
ChesnokovaV.,
DykhuizenD. E.,
OfekI.,
WuX. R.,
KrogfeltK. A.,
StruveC.,
SchembriM. A.,
HastyD. L.1998; Pathogenic adaptation of Escherichia coli by natural variation of the FimH adhesin. Proc Natl Acad Sci U S A 95:8922–8926
SteynB.,
OosthuizenM. C.,
MacDonaldR.,
TheronJ.,
BrözelV. S.2001; The use of glass wool as an attachment surface for studying phenotypic changes in Pseudomonas aeruginosa biofilms by two-dimensional gel electrophoresis. Proteomics 1:871–879
UhlichG. A.,
KeenJ. E.,
ElderR. O.2001; Mutations in the csgD promoter associated with variations in curli expression in certain strains of Escherichia coli O157 : H7. Appl Environ Microbiol 67:2367–2370
VidalO.,
LonginR.,
Prigent-CombaretC.,
DorelC.,
HooremanM.,
LejeuneP.1998; Isolation of an Escherichia coli K-12 mutant strain able to form biofilms on inert surfaces: involvement of a new ompR allele that increases curli expression. J Bacteriol 180:2442–2449
White-ZieglerC. A.,
UmS.,
PérezN. M.,
BernsA. L.,
MalhowskiA. J.,
YoungS.2008; Low temperature (23 °C) increases expression of biofilm-, cold-shock- and RpoS-dependent genes in Escherichia coli K-12. Microbiology 154:148–166
ZhangL.,
FoxmanB.,
MarrsC.2002; Both urinary and rectal Escherichia coli isolates are dominated by strains of phylogenetic group B2. J Clin Microbiol 40:3951–3955