The bfeA (Bordetella ferric enterobactin) receptor gene was cloned from a Bordetella pertussis chromosomal library by using a screen in Escherichia coli to detect iron-repressed genes encoding exported proteins translationally fused to the E. coli phoA gene. The bfeA gene encoded a protein with a molecular mass of approximately 80 kDa and about 50% amino acid sequence identity to both the fepA- and pfe-encoded enterobactin receptors of E. coli and Pseudomonas aeruginosa, respectively. Enterobactin prepared from iron-starved E. coli cultures supported growth of B. pertussis and Bordetella bronchiseptica in the presence of the iron chelator ethylenediamine-di-(o-hydroxyphenylacetic acid) (EDDA). Expression of the bfeA gene was induced by low iron availability, and iron-regulated expression appeared to be dependent upon the presence of the sequence contained within 370 bp upstream of the bfeA structural gene. An internal fragment of the bfeA structural gene and flanking regions were shown by Southern analysis to be highly conserved among Bordetella species. Insertional inactivation of bfeA in both B. pertussis and B. bronchiseptica greatly impaired their ability to grow in the presence of enterobactin and EDDA. These findings suggest that enterobactin produced by other respiratory flora could aid in the colonization of the respiratory tract by Bordetella species.
AgiatoL.-A.,
DyerD.W.1992; Siderophore production and membrane alterations by Bordetella pertussis in reponse to iron starvation.. Infect Immun 60:117–123
Agiato-FosterL.-A.,
DyerD.W.1993; A siderophore production mutant of Bordetella bronchiseptica cannot use lactoferrin as an iron source.. Infect Immun 61:2698–2702
BraunV.,
HantkeK.1991; Genetics of bacterial iron transport.. In Handbook of Microbial Iron Chelates pp. 107–138Winkelmann.G.
Edited by Boca Raton, FL:: CRC Press.;
BraunV.,
SchafferS.,
HantkeK.,
TrogerW.1990; Regulation of gene expression by iron.. In The Molecular Basis of Bacterial Metabolism pp. 164–179HauskaG.,
Thauer.R.
Edited by New York:: Springer.;
BrickmanE.,
BeckwithJ.1975; Analysis of the regulation of Escherichia coli alkaline phosphatase using deletions and 80 transducing phages.. J Mol Biol 96:307–316
BrickmanT.J.,
ArmstrongS.K.1995; Bordetella pertussis fur gene restores iron repressibility of siderophore and protein expression to deregulated Bordetella bronchiseptica mutants.. J Bacteriol 177:268–270
CalderwoodS.B.,
MekalanosJ.J.1987; Iron regulation of Shiga-like toxin expression in Escherichia coli is mediated by the fur locus.. J Bacteriol 169:4759–4764
DeanC.R.,
PooleK.1993b; Expression of the ferric enterobactin receptor (PfeA) of Pseudomonas aeruginosa: involvement of a two-component regulatory system.. Mol Microbiol 8:1095–1103
DriksA.,
RoelsS.,
BeallB.,
MoranC.P.,
LosickR.1994; Subcellular localization of proteins involved in the assembly of the spore coat of Bacillus subtilis.
. Genes & Dev 8:234–244
FortinY.,
PhoenixP.,
DrapeauG.1990; Mutations conferring resistance to azide in Escherichia coli occur primarily in the sec A gene.. J Bacteriol 172:6607–6610
GiladiM.,
ChampionC.L,
HaakeD.A.,
BlancoD.R.,
MillerJ.F.,
MillerJ.N.,
LovettM.E.1993; Use of the 'blue halo' assay in the identification of genes with cleavable signal peptides: cloning of a Borrelia burgdorferi plasmid gene with a signal peptide.. J Bacteriol 175:4129–4136
GorringeA.R.,
WoodsG.,
RobinsonA.1990; Growth and siderophore production by Bordetella pertussis under iron-restricted conditions.. FEMS Microbiol Lett 66:101–106
HeinrichsD.E.,
YoungL.,
PooleK.1991; Pyochelin-mediated iron transport in Pseudomonas aeruginosa-, involvement of a high- molecular mass outer membrane protein.. Infect Immun 59:3680–3684
von KoenigC.H.W.,
TackenA.,
FingerH.1988; Use of supplemented Stainer-Scholte broth for the isolation of Bordetella pertussis from clinical material.. J Clin Microbiol 26:2558–2560
LangmanL.,
YoungI.G.,
FrostG.E.,
RosenburgH.,
GibsonF.1972; Enterochelin system of iron transport in Escherichia coli: mutations affecting ferric-enterochelin esterase.. J Bacteriol 112:1142–1149
LundriganM.D.,
KadnerR.J.1986; Nucleotide sequence of the gene for the ferrienterochelin receptor FepA in Escherichia coli: homology among outer membrane receptors that interact with TonB.. J Biol Chem 261:10797–10801
MenozziF.D.,
GauntiezC.,
LochtC.1991; Identification and purification of transferrin- and lactoferrin-binding proteins of Bordetella pertussis and Bordetella bronchiseptica.
. Infect Immun 59:3982–3988
MeyerJ.M.,
HohnadelD.,
KhanA.,
CorneliusP.1990; Pyoverdin-facilitated iron uptake in Pseudomonas aeruginosa : immunological characterization of the ferripyoverdine receptor.. Mol Microbiol 4:1401–1405
MooreC.H.,
FosterL.-A.,
GerbigD.G.JrDyerD,W.,
GibsonB.W.1995; Identification of alcaligin as the siderophore produced by Bordetella pertussis and Bordetella bronchiseptica.
. J Bacteriol 177:1116–1118
NeilandsJ.B.1981In Development of Iron Chelators for Clinical Use,13MartellA. E.,
AndersonW. F.,
Badman.D. G.
Edited by New York:: Elsevier/North-Holland.;
O’BrienI.G.,
GibsonF.1970; The structure of enterochelin and related 2,3-dihydroxy-IV-benzoylserine conjugates from Escherichia coli.
. Biochim Biophjs Acta 251:393–402
OliverD.B.,
CabelliR.J.,
DolanK.M.,
JarosickG.P.1990; Azide-resistant mutants of Escherichia coli alter the SecA protein, an azide-sensitive component of protein export machinery.. Proc Natl Acad Sci USA878227–8231
PerlmanD.,
HalvorsonH.O.1983; A putative signal peptidase recognition site and sequence in eukaryotic and prokaryotic peptides.. J Mol Biol 167:391–409
RedheadK.,
HillT.,
ChartH.1987; Interaction of transferrin and lactoferrin with the outer membrane of Bordetellapertussis.
. J Gen Microbiol 133:891–898
StojiljkovicI.,
BaumlerA.J.,
HantkeK.1994; Fur regulon in gram negative bacteria: identification and characterization of new iron-regulated Escherichia coli genes by a Fur titration assay.. J Mol Biol 236:531–545
StrauchK.I.,
JohnsonK.,
BeckwithJ.1989; Characterization of degP, a gene required for proteolysis in the cell envelope and essential for growth of Escherichia coli at high temperature.. J Bacteriol 171:2689–2696
StruyveM.,
MoonsM.,
TommassenJ.1991; Carboxy-terminal phenylalanine is essential for the correct assembly of a bacterial outer membrane protein.. J Mol Biol 218:141–148
TaborS.,
RichardsonC.C.1985; A bacteriophage T7 RNA polymerase/promoter system for controlling exclusive expression of specific genes.. Proc Natl Acad Sci USA821074–1078
WayneR.R.,
NeilandsJ.B.1976; Relation of siderophore utilization to colicin receptor activity in mutants of E. coli K-12 resistant to colicins B, V, or la.. Fed Proc 35:1453
WilliamsP.,
MortonD.J.,
TownerK.J.,
StevensonP.,
GriffithsE.1990; Utilization of enterobactin and other exogenous iron sources by Flaemophilus influenzae, H. parainfluen^ae and H. paraphrophilus.
. J Gen Microbiol 136:2343–2350