• We are sorry, but NCBI web applications do not support your browser and may not function properly. More information
Logo of jbacterPermissionsJournals.ASM.orgJournalJB ArticleJournal InfoAuthorsReviewers
J Bacteriol. Jan 1996; 178(2): 496–504.
PMCID: PMC177684

Ferric rhizoferrin uptake into Morganella morganii: characterization of genes involved in the uptake of a polyhydroxycarboxylate siderophore.

Abstract

Iron uptake in Morganella morganii, mediated by the fungal siderophore rhizoferrin, was studied. A Mud1 insertion mutant devoid of growth on ferric rhizoferrin was complemented by a chromosomal DNA fragment of M. morganii that encoded an outer membrane protein and a periplasmic protein named RumA and RumB (for rhizoferrin uptake into Morganella spp.), respectively. rumA and rumB have the same transcription polarity and are probably cotranscribed from an iron-regulated promoter upstream of rumA. A predicted Fur regulatory sequence upstream of rumA was confirmed by the Fur titration assay. At the N terminus of RumA, a putative TonB box contains a proline residue that inactivates TonB-dependent receptors and colicins when introduced at the same position into TonB boxes of Escherichia coli. Analysis of a 10-kb sequence flanking rumA and rumB on both sides revealed seven additional open reading frames for which no role in ferric rhizoferrin uptake could be discerned. Thus, rumA and rumB, both essential for transport of this siderophore, form an isolated operon. Additional genes required for ferric rhizoferrin translocation across the cytoplasmic membrane must map at sites distinct from rumA and rumB. Transport studies revealed that both 55Fe3+ and [3H]ketorhizoferrin are incorporated by M. morganii, demonstrating that rhizoferrin serves as a true iron carrier.

Full Text

The Full Text of this article is available as a PDF (449K).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.
  • Ames GF, Mimura CS, Shyamala V. Bacterial periplasmic permeases belong to a family of transport proteins operating from Escherichia coli to human: Traffic ATPases. FEMS Microbiol Rev. 1990 Aug;6(4):429–446. [PubMed]
  • Bell PE, Nau CD, Brown JT, Konisky J, Kadner RJ. Genetic suppression demonstrates interaction of TonB protein with outer membrane transport proteins in Escherichia coli. J Bacteriol. 1990 Jul;172(7):3826–3829. [PMC free article] [PubMed]
  • Bolivar F, Rodriguez RL, Greene PJ, Betlach MC, Heyneker HL, Boyer HW, Crosa JH, Falkow S. Construction and characterization of new cloning vehicles. II. A multipurpose cloning system. Gene. 1977;2(2):95–113. [PubMed]
  • Braun V, Gross R, Köster W, Zimmermann L. Plasmid and chromosomal mutants in the iron(III)-aerobactin transport system of Escherichia coli. Use of streptonigrin for selection. Mol Gen Genet. 1983;192(1-2):131–139. [PubMed]
  • Casadaban MJ, Cohen SN. Lactose genes fused to exogenous promoters in one step using a Mu-lac bacteriophage: in vivo probe for transcriptional control sequences. Proc Natl Acad Sci U S A. 1979 Sep;76(9):4530–4533. [PMC free article] [PubMed]
  • Eide DJ, Bridgham JT, Zhao Z, Mattoon JR. The vacuolar H(+)-ATPase of Saccharomyces cerevisiae is required for efficient copper detoxification, mitochondrial function, and iron metabolism. Mol Gen Genet. 1993 Nov;241(3-4):447–456. [PubMed]
  • Fecker L, Braun V. Cloning and expression of the fhu genes involved in iron(III)-hydroxamate uptake by Escherichia coli. J Bacteriol. 1983 Dec;156(3):1301–1314. [PMC free article] [PubMed]
  • Friedman AM, Long SR, Brown SE, Buikema WJ, Ausubel FM. Construction of a broad host range cosmid cloning vector and its use in the genetic analysis of Rhizobium mutants. Gene. 1982 Jun;18(3):289–296. [PubMed]
  • Frost GE, Rosenberg H. The inducible citrate-dependent iron transport system in Escherichia coli K12. Biochim Biophys Acta. 1973 Nov 30;330(1):90–101. [PubMed]
  • Fujita N, Mori H, Yura T, Ishihama A. Systematic sequencing of the Escherichia coli genome: analysis of the 2.4-4.1 min (110,917-193,643 bp) region. Nucleic Acids Res. 1994 May 11;22(9):1637–1639. [PMC free article] [PubMed]
  • Gudmundsdottir A, Bell PE, Lundrigan MD, Bradbeer C, Kadner RJ. Point mutations in a conserved region (TonB box) of Escherichia coli outer membrane protein BtuB affect vitamin B12 transport. J Bacteriol. 1989 Dec;171(12):6526–6533. [PMC free article] [PubMed]
  • Günter K, Braun V. In vivo evidence for FhuA outer membrane receptor interaction with the TonB inner membrane protein of Escherichia coli. FEBS Lett. 1990 Nov 12;274(1-2):85–88. [PubMed]
  • Hantke K. Cloning of the repressor protein gene of iron-regulated systems in Escherichia coli K12. Mol Gen Genet. 1984;197(2):337–341. [PubMed]
  • Härle C, Kim I, Angerer A, Braun V. Signal transfer through three compartments: transcription initiation of the Escherichia coli ferric citrate transport system from the cell surface. EMBO J. 1995 Apr 3;14(7):1430–1438. [PMC free article] [PubMed]
  • Heller KJ, Kadner RJ, Günther K. Suppression of the btuB451 mutation by mutations in the tonB gene suggests a direct interaction between TonB and TonB-dependent receptor proteins in the outer membrane of Escherichia coli. Gene. 1988 Apr 15;64(1):147–153. [PubMed]
  • Herrero M, de Lorenzo V, Timmis KN. Transposon vectors containing non-antibiotic resistance selection markers for cloning and stable chromosomal insertion of foreign genes in gram-negative bacteria. J Bacteriol. 1990 Nov;172(11):6557–6567. [PMC free article] [PubMed]
  • Higgins CF. ABC transporters: from microorganisms to man. Annu Rev Cell Biol. 1992;8:67–113. [PubMed]
  • Köster WL, Actis LA, Waldbeser LS, Tolmasky ME, Crosa JH. Molecular characterization of the iron transport system mediated by the pJM1 plasmid in Vibrio anguillarum 775. J Biol Chem. 1991 Dec 15;266(35):23829–23833. [PubMed]
  • Koster M, van Klompenburg W, Bitter W, Leong J, Weisbeek P. Role for the outer membrane ferric siderophore receptor PupB in signal transduction across the bacterial cell envelope. EMBO J. 1994 Jun 15;13(12):2805–2813. [PMC free article] [PubMed]
  • Lundrigan MD, Kadner RJ. 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. 1986 Aug 15;261(23):10797–10801. [PubMed]
  • MacLeod PR, MacLeod RA. Identification and sequence of a Na(+)-linked gene from the marine bacterium Alteromonas haloplanktis which functionally complements the dagA gene of Escherichia coli. Mol Microbiol. 1992 Sep;6(18):2673–2681. [PubMed]
  • Meiwes J, Fiedler HP, Haag H, Zähner H, Konetschny-Rapp S, Jung G. Isolation and characterization of staphyloferrin A, a compound with siderophore activity from Staphylococcus hyicus DSM 20459. FEMS Microbiol Lett. 1990 Jan 15;55(1-2):201–205. [PubMed]
  • Mende J, Braun V. Import-defective colicin B derivatives mutated in the TonB box. Mol Microbiol. 1990 Sep;4(9):1523–1533. [PubMed]
  • Miller VL, Mekalanos JJ. 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. 1988 Jun;170(6):2575–2583. [PMC free article] [PubMed]
  • Neilands JB. Microbial iron compounds. Annu Rev Biochem. 1981;50:715–731. [PubMed]
  • Payne SM. Iron and virulence in the family Enterobacteriaceae. Crit Rev Microbiol. 1988;16(2):81–111. [PubMed]
  • Pilsl H, Glaser C, Gross P, Killmann H, Olschläger T, Braun V. Domains of colicin M involved in uptake and activity. Mol Gen Genet. 1993 Jul;240(1):103–112. [PubMed]
  • Pressler U, Staudenmaier H, Zimmermann L, Braun V. Genetics of the iron dicitrate transport system of Escherichia coli. J Bacteriol. 1988 Jun;170(6):2716–2724. [PMC free article] [PubMed]
  • Sanger F, Nicklen S, Coulson AR. DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci U S A. 1977 Dec;74(12):5463–5467. [PMC free article] [PubMed]
  • Sauer M, Hantke K, Braun V. Sequence of the fhuE outer-membrane receptor gene of Escherichia coli K12 and properties of mutants. Mol Microbiol. 1990 Mar;4(3):427–437. [PubMed]
  • Schöffler H, Braun V. Transport across the outer membrane of Escherichia coli K12 via the FhuA receptor is regulated by the TonB protein of the cytoplasmic membrane. Mol Gen Genet. 1989 Jun;217(2-3):378–383. [PubMed]
  • Smith RL, Thompson LJ, Maguire ME. Cloning and characterization of MgtE, a putative new class of Mg2+ transporter from Bacillus firmus OF4. J Bacteriol. 1995 Mar;177(5):1233–1238. [PMC free article] [PubMed]
  • Stojiljkovic I, Bäumler AJ, Hantke K. Fur regulon in gram-negative bacteria. Identification and characterization of new iron-regulated Escherichia coli genes by a fur titration assay. J Mol Biol. 1994 Feb 18;236(2):531–545. [PubMed]
  • Stokkermans JP, van den Berg WA, van Dongen WM, Veeger C. The primary structure of a protein containing a putative [6Fe-6S] prismane cluster from Desulfovibrio desulfuricans (ATCC 27774). Biochim Biophys Acta. 1992 Aug 17;1132(1):83–87. [PubMed]
  • Struyvé M, Moons M, Tommassen J. Carboxy-terminal phenylalanine is essential for the correct assembly of a bacterial outer membrane protein. J Mol Biol. 1991 Mar 5;218(1):141–148. [PubMed]
  • Tabor S, Richardson CC. A bacteriophage T7 RNA polymerase/promoter system for controlled exclusive expression of specific genes. Proc Natl Acad Sci U S A. 1985 Feb;82(4):1074–1078. [PMC free article] [PubMed]
  • Tam R, Saier MH., Jr Structural, functional, and evolutionary relationships among extracellular solute-binding receptors of bacteria. Microbiol Rev. 1993 Jun;57(2):320–346. [PMC free article] [PubMed]
  • Walter EG, Weiner JH, Taylor DE. Nucleotide sequence and overexpression of the tellurite-resistance determinant from the IncHII plasmid pHH1508a. Gene. 1991 May 15;101(1):1–7. [PubMed]
  • Williams EW, Hawkey PM, Penner JL, Senior BW, Barton LJ. Serious nosocomial infection caused by Morganella morganii and Proteus mirabilis in a cardiac surgery unit. J Clin Microbiol. 1983 Jul;18(1):5–9. [PMC free article] [PubMed]
  • Yanisch-Perron C, Vieira J, Messing J. Improved M13 phage cloning vectors and host strains: nucleotide sequences of the M13mp18 and pUC19 vectors. Gene. 1985;33(1):103–119. [PubMed]

Articles from Journal of Bacteriology are provided here courtesy of American Society for Microbiology (ASM)

Formats:

Related citations in PubMed

See reviews...See all...

Cited by other articles in PMC

See all...

Links

Recent Activity

Your browsing activity is empty.

Activity recording is turned off.

Turn recording back on

See more...