Iron transport systems of Serratia marcescens

Abstract

Serratia marcescens W225 expresses an unconventional iron(III) transport system. Uptake of Fe3+ occurs in the absence of an iron(III)-solubilizing siderophore, of an outer membrane receptor protein, and of the TonB and ExbBD proteins involved in outer membrane transport. The three SfuABC proteins found to catalyze iron(III) transport exhibit the typical features of periplasmic binding-protein-dependent systems for transport across the cytoplasmic membrane. In support of these conclusions, the periplasmic SfuA protein bound iron chloride and iron citrate but not ferrichrome, as shown by protection experiments against degradation by added V8 protease. The cloned sfuABC genes conferred upon an Escherichia coli aroB mutant unable to synthesize its own enterochelin siderophore the ability to grow under iron-limiting conditions (in the presence of 0.2 mM 2.2'-dipyridyl). Under extreme iron deficiency (0.4 mM 2.2'-dipyridyl), however, the entry rate of iron across the outer membrane was no longer sufficient for growth. Citrate had to be added in order for iron(III) to be translocated as an iron citrate complex in a FecA-and TonB-dependent manner through the outer membrane and via SfuABC across the cytoplasmic membrane. FecA-and TonB-dependent iron transport across the outer membrane could be clearly correlated with a very low concentration of iron in the medium. Expression of the sfuABC genes in E. coli was controlled by the Fur iron repressor gene. S. marcescens W225 was able to synthesize enterochelin and take up iron(III) enterochelin. It contained an iron(III) aerobactin transport system but lacked aerobactin synthesis. This strain was able to utilize the hydroxamate siderophores ferrichrome, coprogen, ferrioxamine B, rhodotorulic acid, and schizokinen as sole iron sources and grew on iron citrate as well. In contrast to E. coli K-12, S. marcescens could utilize heme. DNA fragments of the E. coli fhuA, iut, exbB, and fur genes hybridized with chromosomal S. marcescens DNA fragments, whereas no hybridization was obtained between S. marcescens chromosomal DNA and E. colifecA,JhuE, and tonB gene fragments. The presence of multiple iron transport systems was also indicated by the increased synthesis of at least five outer membrane proteins (in the molecular weight range of 72,000 to 87,000) after growth in low-iron media. Serratia liquefaciens and Serratia ficaria produced aerobactin, showing that this siderophore also occurs in the genus Serratia.

Citrate-mediated iron uptake in Pseudomonas aeruginosa: involvement of the citrate-inducible FecA receptor and the FeoB ferrous iron transporter

“…Two operons encoding homologues of Fe 3+ transporters in other bacteria have been annotated in P. aeruginosa, PA5216-5217 (homologue of the HitABC system in Haemophilus influenzae) (Sanders et al, 1994) and PA4687-4688 (homologue of the SfuABC and FbpABC systems in Serratia marcescens and Neisseria spp., respectively) (Adhikari et al, 1996;Angerer et al, 1992). Disruption of PA5216 (45 % identical to HitA) and PA4687 (30 % identical to SfuB) in K2931, yielding the triple knockout strain K2556, did not further compromise citrate-promoted growth in EDDA-containing medium (Fig.…”

Characterization of a ferric‐binding protein mutant in Haemophilus influenzae

“…This coincides with experimental evidence demonstrating that a functional FbpA pathway is independently capable of acquiring cellular iron from ferric-dipyridyl in the periplasm of E. coli (Adhikari et al, 1995) and is the basis on which the closely related sfu operon was cloned and identified (Zimmermann et al, 1989). Genetic and biochemical similarities between the Sfu and Fbp pathways, coupled with the identification of numerous homologues within the Neisseriaceae (N. gonorrhoeae, N. meningitidis), Pasteurellaceae (H. influenzae, Pasteurella haemolytica, Actinobacillus actinomycetemcomitans) and Enterobacteriaceae (Serratia marcescens, Yersinia enterocolitica), suggest that this system represents a common and related mechanism of iron uptake within Gram-negative bacteria (Murray et al, 1991;Angerer et al, 1992;Genco et al, 1994;Sanders et al, 1994;Adhikari et al, 1995;Saken and Heesemann, GenBank submissions). As further periplasmic iron-binding proteins are identified, it would be advantageous to apply a standard non-species-specific nomenclature to describe these homologues, of which the only one in use to date is the term applied by recommendation of the Sixth International Pathogenic Neisseria Conference, ferric binding protein (FbpA; Berish et al, 1990;Confer, 1993).…”

Anion-independent Iron Coordination by the Campylobacter jejuni Ferric Binding Protein

“…These two highly conserved tyrosines may then be used to construct a short sequence motif, (N/Y)XYY, to identify new FbpA family members. Although Asn 200 is not absolutely conserved, because three of 41 FbpAs contain a Tyr substitution, this Tyr is present in the FbpA from Serratia marcescens, which is known to be involved in iron transport (41).…”