This Article Full Text (PDF) Alert me when this article is cited Alert me if a correction is posted Services Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Reprints and Permissions Copyright Information Books from ASM Press MicrobeWorld Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Mills, M. Articles by Payne, S. M. Search for Related Content PubMed PubMed Citation Articles by Mills, M. Articles by Payne, S. M.

 Previous Article  |  Next Article 

J. Bacteriol., 06 1995, 3004-3009, Vol 177, No. 11
Copyright © 1995, American Society for Microbiology

Genetics and regulation of heme iron transport in Shigella dysenteriae and detection of an analogous system in Escherichia coli O157:H7

M Mills and SM Payne
Department of Microbiology, University of Texas at Austin 78712, USA.

Shigella species can use heme as the sole source of iron. In this work, the heme utilization locus of Shigella dysenteriae was cloned and characterized. A cosmid bank of S. dysenteriae serotype 1 DNA was constructed in an Escherichia coli siderophore synthesis mutant incapable of heme transport. A recombinant clone, pSHU12, carrying the heme utilization system of S. dysenteriae was isolated by screening on iron-poor medium supplemented with hemin. Transposon insertional mutagenesis and subcloning identified the region of DNA in pSHU12 responsible for the phenotype of heme utilization. Minicell analysis indicated that a 70-kDa protein encoded by this region was sufficient to allow heme utilization in E. coli. Synthesis of this protein, designated Shu (Shigella heme uptake), was induced by iron limitation. The 70-kDa protein is located in the outer membrane and binds heme, suggesting it is the S. dysenteriae heme receptor. Heme iron uptake was found to be TonB dependent in E. coli. Transformation of an E. coli hemA mutant with the heme utilization subclone, pSHU262, showed that heme could serve as a source of porphyrin as well as iron, indicating that the entire heme molecule is transported into the bacterial cell. DNA sequences homologous to shu were detected in strains of S. dysenteriae serotype 1 and E. coli O157:H7.

This article has been cited by other articles:

• Li, G., Ewers, C., Laturnus, C., Diehl, I., Alt, K., Dai, J., Antao, E.-M., Schnetz, K., Wieler, L. H. (2008). Characterization of a yjjQ mutant of avian pathogenic Escherichia coli (APEC). Microbiology 154: 1082-1093 [Abstract] [Full Text]  
• Burkhard, K. A., Wilks, A. (2007). Characterization of the Outer Membrane Receptor ShuA from the Heme Uptake System of Shigella dysenteriae: SUBSTRATE SPECIFICITY AND IDENTIFICATION OF THE HEME PROTEIN LIGANDS. J. Biol. Chem. 282: 15126-15136 [Abstract] [Full Text]  
• Richard-Fogal, C. L., Frawley, E. R., Feissner, R. E., Kranz, R. G. (2007). Heme Concentration Dependence and Metalloporphyrin Inhibition of the System I and II Cytochrome c Assembly Pathways. J. Bacteriol. 189: 455-463 [Abstract] [Full Text]  
• Schneider, S., Sharp, K. H., Barker, P. D., Paoli, M. (2006). An Induced Fit Conformational Change Underlies the Binding Mechanism of the Heme Transport Proteobacteria-Protein HemS. J. Biol. Chem. 281: 32606-32610 [Abstract] [Full Text]  
• Letoffe, S., Delepelaire, P., Wandersman, C. (2006). The housekeeping dipeptide permease is the Escherichia coli heme transporter and functions with two optional peptide binding proteins. Proc. Natl. Acad. Sci. USA 103: 12891-12896 [Abstract] [Full Text]  
• Lansky, I. B., Lukat-Rodgers, G. S., Block, D., Rodgers, K. R., Ratliff, M., Wilks, A. (2006). The Cytoplasmic Heme-binding Protein (PhuS) from the Heme Uptake System of Pseudomonas aeruginosa Is an Intracellular Heme-trafficking Protein to the {delta}-Regioselective Heme Oxygenase. J. Biol. Chem. 281: 13652-13662 [Abstract] [Full Text]  
• Suits, M. D. L., Pal, G. P., Nakatsu, K., Matte, A., Cygler, M., Jia, Z. (2005). Identification of an Escherichia coli O157:H7 heme oxygenase with tandem functional repeats. Proc. Natl. Acad. Sci. USA 102: 16955-16960 [Abstract] [Full Text]  
• Wyckoff, E. E., Lopreato, G. F., Tipton, K. A., Payne, S. M. (2005). Shigella dysenteriae ShuS Promotes Utilization of Heme as an Iron Source and Protects against Heme Toxicity. J. Bacteriol. 187: 5658-5664 [Abstract] [Full Text]  
• Shima, K., Terajima, J., Sato, T., Nishimura, K., Tamura, K., Watanabe, H., Takeda, Y., Yamasaki, S. (2004). Development of a PCR-Restriction Fragment Length Polymorphism Assay for the Epidemiological Analysis of Shiga Toxin-Producing Escherichia coli. J. Clin. Microbiol. 42: 5205-5213 [Abstract] [Full Text]  
• Vanderpool, C. K., Armstrong, S. K. (2004). Integration of Environmental Signals Controls Expression of Bordetella Heme Utilization Genes. J. Bacteriol. 186: 938-948 [Abstract] [Full Text]  
• Karmali, M. A., Mascarenhas, M., Shen, S., Ziebell, K., Johnson, S., Reid-Smith, R., Isaac-Renton, J., Clark, C., Rahn, K., Kaper, J. B. (2003). Association of Genomic O Island 122 of Escherichia coli EDL 933 with Verocytotoxin-Producing Escherichia coli Seropathotypes That Are Linked to Epidemic and/or Serious Disease. J. Clin. Microbiol. 41: 4930-4940 [Abstract] [Full Text]  
• Garrido, M. E., Bosch, M., Medina, R., Bigas, A., Llagostera, M., Perez de Rozas, A. M., Badiola, I., Barbe, J. (2003). fur-independent regulation of the Pasteurella multocida hbpA gene encoding a haemin-binding protein. Microbiology 149: 2273-2281 [Abstract] [Full Text]  
• Allison, H. E., Sergeant, M. J., James, C. E., Saunders, J. R., Smith, D. L., Sharp, R. J., Marks, T. S., McCarthy, A. J. (2003). Immunity Profiles of Wild-Type and Recombinant Shiga-Like Toxin-Encoding Bacteriophages and Characterization of Novel Double Lysogens. Infect. Immun. 71: 3409-3418 [Abstract] [Full Text]  
• Ashour, J., Hondalus, M. K. (2003). Phenotypic Mutants of the Intracellular Actinomycete Rhodococcusequi Created by In Vivo Himar1 Transposon Mutagenesis. J. Bacteriol. 185: 2644-2652 [Abstract] [Full Text]  
• Vanderpool, C. K., Armstrong, S. K. (2003). Heme-Responsive Transcriptional Activation of Bordetella bhu Genes. J. Bacteriol. 185: 909-917 [Abstract] [Full Text]  
• Battistoni, F., Platero, R., Duran, R., Cervenansky, C., Battistoni, J., Arias, A., Fabiano, E. (2002). Identification of an Iron-Regulated, Hemin-Binding Outer Membrane Protein in Sinorhizobium meliloti. Appl. Environ. Microbiol. 68: 5877-5881 [Abstract] [Full Text]  
• Murphy, E. R., Sacco, R. E., Dickenson, A., Metzger, D. J., Hu, Y., Orndorff, P. E., Connell, T. D. (2002). BhuR, a Virulence-Associated Outer Membrane Protein of Bordetella avium, Is Required for the Acquisition of Iron from Heme and Hemoproteins. Infect. Immun. 70: 5390-5403 [Abstract] [Full Text]  
• Blanc-Potard, A.-B., Tinsley, C., Scaletsky, I., Le Bouguenec, C., Guignot, J., Servin, A. L., Nassif, X., Bernet-Camard, M.-F. (2002). Representational Difference Analysis between Afa/Dr Diffusely Adhering Escherichia coli and Nonpathogenic E. coli K-12. Infect. Immun. 70: 5503-5511 [Abstract] [Full Text]  
• Torres, A. G., Redford, P., Welch, R. A., Payne, S. M. (2001). TonB-Dependent Systems of Uropathogenic Escherichia coli: Aerobactin and Heme Transport and TonB Are Required for Virulence in the Mouse. Infect. Immun. 69: 6179-6185 [Abstract] [Full Text]  
• Purdy, G. E., Payne, S. M. (2001). The SHI-3 Iron Transport Island of Shigella boydii 0-1392 Carries the Genes for Aerobactin Synthesis and Transport. J. Bacteriol. 183: 4176-4182 [Abstract] [Full Text]  
• Vanderpool, C. K., Armstrong, S. K. (2001). The Bordetella bhu Locus Is Required for Heme Iron Utilization. J. Bacteriol. 183: 4278-4287 [Abstract] [Full Text]  
• Xu, X., Holt, S. C., Kolodrubetz, D. (2001). Cloning and Expression of Two Novel Hemin Binding Protein Genes from Treponema denticola. Infect. Immun. 69: 4465-4472 [Abstract] [Full Text]  
• Ye, C., Xu, J. (2001). Prevalence of Iron Transport Gene on Pathogenicity-Associated Island of Uropathogenic Escherichia coli in E. coli O157:H7 Containing Shiga Toxin Gene. J. Clin. Microbiol. 39: 2300-2305 [Abstract] [Full Text]  
• Henderson, D. P., Wyckoff, E. E., Rashidi, C. E., Verlei, H., Oldham, A. L. (2001). Characterization of the Plesiomonas shigelloides Genes Encoding the Heme Iron Utilization System. J. Bacteriol. 183: 2715-2723 [Abstract] [Full Text]  
• Nagy, G., Dobrindt, U., Kupfer, M., Emody, L., Karch, H., Hacker, J. (2001). Expression of Hemin Receptor Molecule ChuA Is Influenced by RfaH in Uropathogenic Escherichia coli Strain 536. Infect. Immun. 69: 1924-1928 [Abstract] [Full Text]  
• Schmitt, M. P., Drazek, E. S. (2001). Construction and Consequences of Directed Mutations Affecting the Hemin Receptor in Pathogenic Corynebacterium Species. J. Bacteriol. 183: 1476-1481 [Abstract] [Full Text]  
• Reeves, S. A., Torres, A. G., Payne, S. M. (2000). TonB Is Required for Intracellular Growth and Virulence of Shigella dysenteriae. Infect. Immun. 68: 6329-6336 [Abstract] [Full Text]  
• Clermont, O., Bonacorsi, S., Bingen, E. (2000). Rapid and Simple Determination of the Escherichia coli Phylogenetic Group. Appl. Environ. Microbiol. 66: 4555-4558 [Abstract] [Full Text]  
• Wilks, A., Moenne-Loccoz, P. (2000). Identification of the Proximal Ligand His-20 in Heme Oxygenase (Hmu O) from Corynebacterium diphtheriae. OXIDATIVE CLEAVAGE OF THE HEME MACROCYCLE DOES NOT REQUIRE THE PROXIMAL HISTIDINE. J. Biol. Chem. 275: 11686-11692 [Abstract] [Full Text]  
• Simpson, W., Wang, C.-Y., Mikolajczyk-Pawlinska, J., Potempa, J., Travis, J., Bond, V. C., Genco, C. A. (1999). Transposition of the Endogenous Insertion Sequence Element IS1126 Modulates Gingipain Expression in Porphyromonas gingivalis. Infect. Immun. 67: 5012-5020 [Abstract] [Full Text]  
• Schmitt, M. P. (1999). Identification of a Two-Component Signal Transduction System from Corynebacterium diphtheriae That Activates Gene Expression in Response to the Presence of Heme and Hemoglobin. J. Bacteriol. 181: 5330-5340 [Abstract] [Full Text]  
• Thompson, J. M., Jones, H. A., Perry, R. D. (1999). Molecular Characterization of the Hemin Uptake Locus (hmu) from Yersinia pestis and Analysis of hmu Mutants for Hemin and Hemoprotein Utilization. Infect. Immun. 67: 3879-3892 [Abstract] [Full Text]  
• Chu, G. C., Katakura, K., Zhang, X., Yoshida, T., Ikeda-Saito, M. (1999). Heme Degradation as Catalyzed by a Recombinant Bacterial Heme Oxygenase (Hmu O) from Corynebacterium diphtheriae. J. Biol. Chem. 274: 21319-21325 [Abstract] [Full Text]  
• Turner, P. C., Thomas, C. E., Elkins, C., Clary, S., Sparling, P. F. (1998). Neisseria gonorrhoeae Heme Biosynthetic Mutants Utilize Heme and Hemoglobin as a Heme Source but Fail To Grow within Epithelial Cells. Infect. Immun. 66: 5215-5223 [Abstract] [Full Text]  
• Thomas, C. E., Olsen, B., Elkins, C. (1998). Cloning and Characterization of tdhA, a Locus Encoding a TonB-Dependent Heme Receptor from Haemophilus ducreyi. Infect. Immun. 66: 4254-4262 [Abstract] [Full Text]  
• Cope, L. D., Thomas, S. E., Hrkal, Z., Hansen, E. J. (1998). Binding of Heme-Hemopexin Complexes by Soluble HxuA Protein Allows Utilization of This Complexed Heme by Haemophilus influenzae. Infect. Immun. 66: 4511-4516 [Abstract] [Full Text]  
• Khun, H. H., Kirby, S. D., Lee, B. C. (1998). A Neisseria meningitidis fbpABC Mutant Is Incapable of Using Nonheme Iron for Growth. Infect. Immun. 66: 2330-2336 [Abstract] [Full Text]  
• Wilks, A., Schmitt, M. P. (1998). Expression and Characterization of a Heme Oxygenase (Hmu O) from Corynebacterium diphtheriae. IRON ACQUISITION REQUIRES OXIDATIVE CLEAVAGE OF THE HEME MACROCYCLE. J. Biol. Chem. 273: 837-841 [Abstract] [Full Text]  
• Nataro, J. P., Kaper, J. B. (1998). Diarrheagenic Escherichia coli. Clin. Microbiol. Rev. 11: 142-201 [Abstract] [Full Text]  
• Elkins, C., Totten, P. A., Olsen, B., Thomas, C. E. (1998). Role of the Haemophilus ducreyi Ton System in Internalization of Heme from Hemoglobin. Infect. Immun. 66: 151-160 [Abstract] [Full Text]  
• Chu, G. C., Katakura, K., Tomita, T., Zhang, X., Sun, D., Sato, M., Sasahara, M., Kayama, T., Ikeda-Saito, M., Yoshida, T. (2000). Histidine 20, the Crucial Proximal Axial Heme Ligand of Bacterial Heme Oxygenase Hmu O from Corynebacterium diphtheriae. J. Biol. Chem. 275: 17494-17500 [Abstract] [Full Text]