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1.B.14 The Outer Membrane Receptor (OMR) Family

The OMR family includes a large number of sequenced Gram-negative bacterial outer membrane proteins which form transmembrane pores and transport relatively large molecules from the external milieu to the periplasm in an energized process. Although represented in cyanobacteria, no OMR member has been identified in a Gram-positive bacterium, an archaeon or a eukaryote. Energization of transport across the outer membrane requires a heterotrimeric complex of proteins, the TonB-ExbB-ExbD complex, or in some cases, the TolA-TolQ-TolR complex (TC #10.6). Energization requires the proton motive force (pmf) across the cytoplasmic membrane. In the absence of a pmf or one of the three energy coupling proteins of the complex, the receptor binds its substrate, but transport does not occur. Substrates transported by OMR family members include iron-siderophore complexes, vitamin B12, Cu2+, colicins (group B colicins are transported via TonB-dependent receptors while group A colicins are transported via TolA-dependent receptors), and the DNA of various phage. OMR proteins are also essential for the utilization of iron from eukaryotic proteins such as transferrin, hemoglobin and hemin. The vitamin B12, and iron-siderophore receptors feed into ABC-type permeases (TC #3.A.1.13 and 3.A.1.14) for transport across the cytoplasmic membrane. Alteration (e.g., small internal deletions) of some OMR members can convert them into diffusion channels. Normally, they probably form ligand-specific and energy-gated pores through the outer membranes of Gram-negative bacteria. However, the fact that minor genetic changes result in the generation of diffusion channels suggests that these proteins form large porin-like β-barrel structures.

The three-dimensional structure of one OMR family member, FhuA (TC #1.B.14.1.4), has been elucidated in two conformations, one with and one without bound ferrichrome-iron, both at about 2.6 = resolution (see Ferguson and Deisenhofer (2004) for a review summarizing function/structure relationships). FhuA is a β-barrel composed of 22 antiparallel β-strands. In contrast to the trimeric arrangement seen in most porins, FhuA is monomeric. Located within the β-barrel is a domain called the 'cork' which consists of a four-stranded β-sheet and four short α-helices. The cork closes the channel, but without the cork, there is no activity (Braun et al., 2003). The barrel and cork can be synthesized as separate polypeptide chains, and activity is still observed. The β-barrel is made first, and the cork is inserted later, extracytoplasmically (Braun et al., 2003). A single lipopolysaccharide is tightly associated with the transmembrane region of FhuA. Upon binding of ferrichrome-iron in an aromatic pocket near the cell surface, conformational changes are transduced to the periplasmic face of FhuA, signaling ligand-loading. Based on these findings, a structural model for TonB-dependent, FhuA-mediated siderophore-iron transport across the outer membrane of E. coli has been proposed. Substrate binding induces long-range structural changes that involve gating (Braun and Braun, 2002). Moreover, a ternary complex of FhuA, TonB and FhuD (the periplasmic ABC-type binding receptor) has been demonstrated (Carter et al., 2006). FhuD accepts ferrichrome from FhuA and passes it on to its ABC transporter. Some of these transporters are involved in siderophore-mediated signaling cascades that sense signals at the cell surface and control transcription of genes encoding proteins for siderophore transport and biosynthesis (Braun and Braun, 2002).

Three structures of the Serratia marcescens receptor, HasR (1.B.14.5.1) in complex with its hemophore HasA, have been solved (Krieg et al., 2009). The transfer of heme over a distance of 9 A from its high-affinity site in HasA into a site of lower affinity in HasR is coupled with the exergonic complex formation of the 2 proteins. Upon docking to the receptor, 1 of the 2 axial heme coordinations of the hemophore is initially broken, but the position and orientation of the heme is preserved. Subsequently, steric displacement of heme by a receptor residue ruptures the other axial coordination, leading to heme transfer into the receptor (Krieg et al., 2009).

OprC of Pseudomonas aeruginosa and NosA of P. stutzeri are two large outer membrane receptors that exhibit copper-binding (Kd = 2.6 µM), channel-forming, and Cu2+ transporting characteristics. Liposome swelling assays with the purified protein and planar bilayer ion conductance measurements suggest that OprC forms small channels after the precursors form (723 aas) is processed to the mature form (668 aas). NosA of P. stutzeri is 65% identical to OprC, and it conveys Cu2+ to intracellular acceptors. OprC synthesis is repressed by exogenous Cu2+ and derepressed by anaerobiosis in the presence of nitrate, results consistent with the conclusion that both it and NosA are involved in copper utilization.

Both one- and two-component TonB-dependent transport systems are known. Most OMRs are single-component systems and are analogous to the well-characterized siderophore receptors (TC #1.B.14.1.1-1.B.14.1.4 below). Two component systems consist of a TonB-dependent receptor homologous to those of the one component systems as well as an accessory lipoprotein. The HpuAB pair (TC #9.14.2.4 below) is one example of such a system, while the TbpAB (TC #1.B.14.2.1) and the LbpAB (TC #1.B.14.2.5) systems are two other examples. The LbpB and TbpB lipoproteins are homologous, but the smaller HpuA lipoprotein is not demonstrably homologous to either LbpB and TbpB.

The HasR receptors of Serratia marcescens and Pseudomonas aeruginosa use an extracellular processed haemophore, HasA, that captures free or haemoglobin-bound haem and shuttles it to HasR in preparation for transport across the outer membrane by a TonB-dependent mechanism. HasA is a monomeric protein that binds haem with very high affinity (Kd lower than 10-8 M) and binds HasR both in the heme-free and heme-loaded forms with a Kd of about 10-10. It is exported via an ABC-type export system. The iron-regulated iron-siderophore yersiniabactin receptors are also the pesticin receptors of Yersinia species which provide the route entry of the bacteriocin, pesticin.

Wolff et al. (2007) reported the 3-D NMR structure of apoHasA and the backbone dynamics of both loaded and unloaded hemophore. While the overall structure of HasA is very similar in the apo and holo forms, the hemophore presents a transition from an open to a closed form upon ligand binding, through a large movement, of up to 30 A, of loop L1 bearing H32. Comparison of loaded and unloaded HasA dynamics on different time scales reveals striking flexibility changes in the binding pocket. These features provide the dual function of heme binding and release to the HasR receptor (Wolff et al., 2007).

The structure of the BtuB outer membrane receptor (OMR; 1.B.14.3.1) and the FhuA OMR (1.B.14.1.4) complexed with the C-terminal domain of TonB (2.C.1.1.1), the energy transmitter to the OMR from the ExbBD energizer, shows TonB binding to the TonB box in the OMRs. TonB binding causes the TonB box to form a β-strand, forming a β-sheet with TonB's own β-strand. This is consistent with a mechanical 'pulling' mechanism of transport (Shultis et al., 2006). The conserved TonB arginine 166 is oriented to form multiple contacts with the FhuA 'cork', the globublar domain enclosed by the β-barrel (Pawelek et al., 2006).


Transport results from energy-driven movement of the TonB protein, which either pulls the plug out of the barrel or causes it to rearrange within the barrel. Udho et al. (2009) discovered that if the cis solution contains 4 M urea, then, with the periplasmic side of the channel facing that solution, macroscopic conductances and single channel events can be observed with FhuA, Cir, and BtuB. Channels generated by 4 M urea exposure were not a consequence of general protein denaturation as their ligand-binding properties were preserved. Thus, with FhuA, addition of ferrichrome (its siderophore) to the trans, extracellular-facing side reversibly inhibited 4 M urea-induced channel opening while blocking the channel (Shultis et al., 2006). With Cir, addition of colicin Ia (the microbial toxin that targets Cir) to the trans, extracellular-facing side, prevented 4 M urea-induced channel opening. Maybe 4 M urea reversibly unfolds the plugs, thereby opening an ion-conducting pathway through these channels. This might mimic the in vivo action of TonB on these plugs (Udho et al., 2009).

TonB-dependent transporters bind and transport ferric chelates, vitamin B12, nickel complexes, and carbohydrates. The transport process requires energy in the form of the pmf and the TonB-ExbB-ExbD complex to transduce this energy to the outer membrane. The siderophore substrates range in complexity from simple small molecules such as citrate to large proteins such as serum transferrin and hemoglobin. Expression can be regulated by metal-dependent regulators, σ/anti-σ factors, small RNAs, and a riboswitch (Noinaj et al., 2010). Noinaj et al. (2010) summarized the regulation, structure and function of these systems.

The generalized transport reaction for proteins of the OMR family is:

Substrate (out) Substrate (periplasm).

 

References associated with 1.B.14 family:

Adams, H., G. Zeder-Lutz, I. Schalk, F. Pattus, and H. Celia. (2006). Interaction of TonB with the outer membrane receptor FpvA of Pseudomonas aeruginosa. J. Bacteriol. 188: 5752-5761. 16885443
Alice, A.F., C.S. Lopez, C.A. Lowe, M.A. Ledesma, and J.H. Crosa. (2006). Genetic and transcriptional analysis of the siderophore malleobactin biosynthesis and transport genes in the human pathogen Burkholderia pseudomallei K96243. J. Bacteriol. 188: 1551-1566. 16452439
Amarelle, V., M.R. O'Brian, and E. Fabiano. (2008). ShmR is essential for utilization of heme as a nutritional iron source in Sinorhizobium meliloti. Appl. Environ. Microbiol. 74: 6473-6475. 18757569
Baysse, C., J.-M. Meyer, P. Plesiat, V. Geoffroy, Y. Michel-Briand, and P. Cornelis. (1999). Uptake of pyocin S3 occurs through the outer membrane ferripyoverdine type II receptor of Pseudomonas aeruginosa. J. Bacteriol. 181: 3849-3851. 10368165
Benevides-Matos N. and Biville F. (2010). The Hem and Has haem uptake systems in Serratia marcescens. Microbiology. 156(Pt 6):1749-57. 20299406
Benevides-Matos, N., C. Wandersman, and F. Biville. (2008). HasB, the Serratia marcescens TonB paralog, is specific to HasR. J. Bacteriol. 190(1):21-7. 17951376
Bhat, S., X. Zhu, R.P. Patel, R. Orlando, and L.J. Shimkets. (2011). Identification and localization of Myxococcus xanthus porins and lipoproteins. PLoS One 6: e27475. 22132103
Braud, A., M. Hannauer, G.L. Mislin, and I.J. Schalk. (2009). The Pseudomonas aeruginosa pyochelin-iron uptake pathway and its metal specificity. J. Bacteriol. 191: 3517-3525. 19329644
Braun, M., F. Endriss, H. Killmann, and V. Braun. (2003). In vivo reconstitution of the FhuA transport protein of Escherichia coli K-12. J. Bacteriol. 185: 5508-5518. 12949103
Braun, V. and H. Killmann. (1999). Bacterial solutions to the iron-supply problem. Trends Biochem. Sci. 24: 104-109. 10203757
Braun, V. and M. Braun. (2002). Iron transport and signaling in Escherichia coli. FEBS Lett. 529: 78-85. 12354617
Braun, V., A. Pramanik, T. Gwinner, M. Köberle, and E. Bohn. (2009). Sideromycins: tools and antibiotics. Biometals 22: 3-13. 19130258
Braun, V., H. Pilsl, and P. Gross. (1994). Colicins: structures, modes of action, transfer through membranes and evolution. Arch. Microbiol. 161: 199-206. 8161282
Braun, V., K. Hantke, and W. Köster. (1998). Bacterial iron transport: mechanisms, genetics, and regulation. In Metal Ions in Biological Systems, Vol. 35, Chapter 3, A. Sigel and H. Sigel (Eds.), Marcel Dekker, Inc., New York. 9444760
Brickman, T.J., C.K. Vanderpool, and S.K. Armstrong. (2006). Heme transport contributes to in vivo fitness of Bordetella pertussis during primary infection in mice. Infect. Immun. 74: 1741-1744. 16495546
Cadieux, N., N. Barekzi, and C. Bradbeer. (2007). Observations on the Calcium Dependence and Reversibility of Cobalamin Transport across the Outer Membrane of Escherichia coli. J. Biol. Chem. 282(48): 34921-34928. 17908684
Carswell, C.L., M.D. Rigden, and J.E. Baenziger. (2008). Expression, purification, and structural characterization of CfrA, a putative iron transporter from Campylobacter jejuni. J. Bacteriol. 190: 5650-5662. 18556796
Carter, D.M., I.R. Miousse, J.N. Gagnon, E. Martinez, A. Clements, J. Lee, M.A. Hancock, H. Gagnon, P.D. Pawelek, and J.W. Coulton. (2006). Interactions between TonB from Escherichia coli and the periplasmic protein FhuD. J. Biol. Chem. 281: 35413-35424. 16928679
Cho, K.H. and A.A. Salyers. (2001). Biochemical analysis of interactions between outer membrane proteins that contribute to starch utilization by Bacteroides thetaiotaomicron. J. Bacteriol. 183: 7224-7230. 11717282
Cobessi, D., A. Meksem, and K. Brillet. (2010). Structure of the heme/hemoglobin outer membrane receptor ShuA from Shigella dysenteriae: heme binding by an induced fit mechanism. Proteins 78: 286-294. 19731368
Curtis, N.A., R.L. Eisenstadt, S.J. East, R.J. Cornford, L.A. Walker,and A.J. White. (1988). Iron-regulated outer membrane proteins of Escherichia coli K-12 and mechanism of action of catechol-substituted cephalosporins. Antimicrob. Agents Chemother. 32: 1879-1886. 3072926
Eisenbeis, S., S. Lohmiller, M. Valdebenito, S. Leicht, and V. Braun. (2008). NagA-dependent uptake of N-acetyl-glucosamine and N-acetyl-chitin oligosaccharides across the outer membrane of Caulobacter crescentus. J. Bacteriol. 190: 5230-5238. 18539735
Ferguson, A.D. and J. Deisenhofer. (2004). Metal import through microbial membranes. Cell 116: 15-24. 14718163
Ferguson, A.D., E. Hofmann, J.W. Coulton, K. Diederichs, and W. Welte. (1998). Siderophore-mediated iron transport: crystal structure of FhuA with bound lipopolysaccharide. Science 282: 2215-2220. 9856937
Ferreira, M.J. and I. Sá-Nogueira. (2010). A multitask ATPase serving different ABC-type sugar importers in Bacillus subtilis. J. Bacteriol. 192: 5312-5318. 20693325
Fetherston, J.D., J.W. Lillard, Jr., and R.D. Perry. (1995). Analysis of the pesticin receptor from Yersinia pestis: role in iron-deficient growth and possible regulation by its siderophore. J. Bacteriol. 177: 1824-1833. 7896707
Folschweiller, N., I.J. Schalk, H. Celia, B. Kieffer, M.A. Abdallah, and F. Pattus. (2000). The pyoverdin receptor FpvA, a TonB-dependent receptor involved in iron uptake by Pseudomonas aeruginosa. Mol. Membr. Biol. 17: 123-133. 11128971
Forman, S., M.J. Nagiec, J. Abney, R.D. Perry, and J.D. Fetherston. (2007). Analysis of the aerobactin and ferric hydroxamate uptake systems of Yersinia pestis. Microbiology. 153: 2332-2341. 17600077
Franza, T., B. Mahé, and D. Expert. (2005). Erwinia chrysanthemi requires a second iron transport route dependent of the siderophore achromobactin for extracellular growth and plant infection. Mol. Microbiol. 55: 261-275. 15612933
Fusco, W.G., N. Choudhary, S. Council, E. Collins, and I. Leduc. (2013). Mutational analysis of hemoglobin binding and heme utilization by a bacterial hemoglobin receptor. J. Bacteriol. [Epub: Ahead of Print] 23667232
Gouaux, E. (1997). The long and short of colicin action: the molecular basis for the biological activity of channel-forming colicins. Structure 5: 313-317. 9083116
Hancock, V., L. Ferrières, and P. Klemm. (2008). The ferric yersiniabactin uptake receptor FyuA is required for efficient biofilm formation by urinary tract infectious Escherichia coli in human urine. Microbiology. 154: 167-175. 18174135
Hantke, K., (1990). Dihydroxybenzoylserine--a siderophore for E. coli. FEMS Microbiol, Lett. 55: 5-8. 2139424
Izadi-Pruneyre, N., F. Huché, G.S. Lukat-Rodgers, A. Lecroisey, R. Gilli, K.R. Rodgers, C. Wandersman, and P. Delepelaire. (2006). The heme transfer from the soluble HasA hemophore to its membrane-bound receptor HasR is driven by protein-protein interaction from a high to a lower affinity binding site. J. Biol. Chem. 281: 25541-25550. 16774915
Jakes, K.S. and A. Finkelstein. (2010). The colicin Ia receptor, Cir, is also the translocator for colicin Ia. Mol. Microbiol. 75: 567-578. 19919671
Killmann, H., R. Benz, and B. Braun. (1993). Conversion of the FhuA transport protein into a diffusion channel through the outer membrane of Escherichia coli. EMBO J. 12: 3007-3016. 7688295
Kornreich-Leshem, H., C. Ziv, E. Gumienna-Kontecka, R. Arad-Yellin, Y. Chen, M. Elhabiri, A.M. Albrecht-Gary, Y. Hadar, and A. Shanzer. (2005). Ferrioxamine B analogues: targeting the FoxA uptake system in the pathogenic Yersinia enterocolitica. J. Am. Chem. Soc. 127: 1137-1145. 15669853
Krieg, S., F. Huché, K. Diederichs, N. Izadi-Pruneyre, A. Lecroisey, C. Wandersman, P. Delepelaire, and W. Welte. (2009). Heme uptake across the outer membrane as revealed by crystal structures of the receptor-hemophore complex. Proc. Natl. Acad. Sci. USA 106: 1045-1050. 19144921
López, C.S. and J.H. Crosa. (2007). Characterization of ferric-anguibactin transport in Vibrio anguillarum. Biometals 20: 393-403. 17287889
Leach, L.H. and T.A. Lewis. (2006). Identification and characterization of Pseudomonas membrane transporters necessary for utilization of the siderophore pyridine-2,6-bis(thiocarboxylic acid) (PDTC). Microbiology 152: 3157-3166. 17005994
Lefèvre, J., P. Delepelaire, M. Delepierre, and N. Izadi-Pruneyre. (2008). Modulation by substrates of the interaction between the HasR outer membrane receptor and its specific TonB-like protein, HasB. J. Mol. Biol. 378: 838-849. 18402979
Létoffé, S., F. Nato, M.E. Goldberg, and C. Wandersman. (1999). Interactions of HasA, a bacterial haemophore, with haemoglobin and with its outer membrane receptor HasR. Mol. Microbiol. 33: 546-555. 10417645
Létoffé, S., K. Omori, and C. Wandersman. (2000). Functional characterization of the HasAPF hemophore and its truncated and chimeric variants: determination of a region involved in binding to the hemophore receptor. J. Bacteriol. 182: 4401-4405. 10913071
Lewis, L.A., M. Gipson, K. Hartman, T. Ownbey, J. Vaughn, and D.W. Dyer. (1999). Phase variation of HpuAB and HmbR, two distinct haemoglobin receptors of Neisseria meningitidis DNM2. Mol. Microbiol. 32: 977-989. 10361300
Lewis, L.A., M.-H. Sung, M. Gipson, K. Hartman, and D.W. Dyer. (1998). Transport of intact porphyrin by HpuAB, the hemoglobin-haptoglobin utilization system of Neisseria meningitidis. J. Bacteriol. 180: 6043-6047. 9811666
Locher, K.P., B. Rees, R. Koebnik, A. Mitschler, L. Moulinier, J.P. Rosenbusch, and D. Moras. (1998). Transmembrane signaling across the ligand-gated FhuA receptor: crystal structures of free and ferrichrome-bound states reveal allosteric changes. Cell 95: 771-778. 9865695
Lohmiller, S., K. Hantke, S.I. Patzer, and V. Braun. (2008). TonB-dependent maltose transport by Caulobacter crescentus. Microbiology 154: 1748-1754. 18524929
Lynch, D., J. O’Brien, T. Welch, P. Clarke, P.O. Cuív, J.H. Crosa, and M. O’Connell. (2001). Genetic organization of the region encoding regulation, biosynthesis, and transport of rhizobactin 1021, a siderophore produced by Sinorhizobium meliloti. J. Bacteriol. 183: 2576-2585. 11274118
Marshall, B., A. Stintzi, C. Gilmour, J.M. Meyer, and K. Poole. (2009). Citrate-mediated iron uptake in Pseudomonas aeruginosa: involvement of the citrate-inducible FecA receptor and the FeoB ferrous iron transporter. Microbiology 155: 305-315. 19118371
Michel, L., A. Bachelard, and C. Reimmann. (2007). Ferripyochelin uptake genes are involved in pyochelin-mediated signalling in Pseudomonas aeruginosa. Microbiology 153: 1508-1518. 17464065
Mokdad, A., D.Z. Herrick, A.K. Kahn, E. Andrews, M. Kim, and D.S. Cafiso. (2012). Ligand-Induced Structural Changes in the Escherichia coli Ferric Citrate Transporter Reveal Modes for Regulating Protein-Protein Interactions. J. Mol. Biol. 423: 818-830. 22982293
Morin, N., I. Lanneluc, N. Connil, M. Cottenceau, A.M. Pons, and S. Sablé. (2011). Mechanism of Bactericidal Activity of Microcin L in Escherichia coli and Salmonella enterica. Antimicrob. Agents Chemother. 55: 997-1007. 21189348
Nader, M., L. Journet, A. Meksem, L. Guillon, and I.J. Schalk. (2011). Mechanism of ferripyoverdine uptake by Pseudomonas aeruginosa outer membrane transporter FpvA: no diffusion channel formed at any time during ferrisiderophore uptake. Biochemistry 50: 2530-2540. 21329359
Nader, M., W. Dobbelaere, M. Vincent, L. Journet, H. Adams, D. Cobessi, J. Gallay, and I.J. Schalk. (2007). Identification of residues of FpvA involved in the different steps of Pvd-Fe uptake in Pseudomonas aeruginosa. Biochemistry 46: 11707-11717. 17900151
Nau, C.D. and J. Konisky. (1989). Evolutionary relationship between the TonB-dependent outer membrane transport proteins: nucleotide and amino-acid sequences of the Escherichia coli colicin I receptor gene. J. Bacteriol. 171: 1041-1047. 2644220
Olczak T., A. Sroka, J. Potempa, M. Olczak. (2007). Porphyromonas gingivalis HmuY and HmuR: further characterization of a novel mechanism of heme utilization. Arch Microbiol. 17922109
Olczak, T., D.W. Dixon, and C.A. Genco. (2001). Binding specificity of the Porphyromonas gingivalis heme and hemoglobin receptor HmuR, gingipain K, and gingipain R1 for heme, porphyrins, and metalloporphyrins. J. Bacteriol. 183: 5599-5608. 11544222
Pawelek, P.D., N. Croteau, C. Ng-Thow-Hing, C.M. Khursigara, N. Moiseeva, M. Allaire, and J.W. Coulton. (2006). Structure of TonB in complex with FhuA, E. coli outer membrane receptor. Science 312: 1399-1402. 16741125
Postle, K. (1993). TonB protein and energy transduction between membranes. J. Bioenerg. Biomembr. 25: 591-601. 8144488
Postle, K. and R.J. Kadner. (2003). Touch and go: tying TonB to transport. Mol. Microbiol. 49: 869-882. 12890014
Prinz, T., M. Meyer, A. Pettersson, and J. Tommassen. (1999). Structural characterization of the lactoferrin receptor from Neisseria meningitidis. J. Bacteriol. 181: 4417-4419. 10400602
Rabsch, W., W. Voight, R. Reissbrodt, R.M. Tsolis, and A.J. Bäumler. (1999). Salmonella typhimurium IroN and FepA proteins mediate uptake of enterobactin but differ in their specificity for other siderophores. J. Bacteriol. 181: 3610-3612. 10348879
Reeves, A.R., G.R. Wang, and A.A. Salyers. (1997). Characterization of four outer membrane proteins that play a role in utilization of starch by Bacteroides thetaiotaomicron. J. Bacteriol. 179: 643-649. 9006015
Rodionov, D.A., A.G. Vitreschak, A.A. Mironov, and M.S. Gelfand. (2002). Comparative genomics of thiamin biosynthesis in procaryotes. New genes and regulatory mechanisms. J. Biol. Chem. 277: 48949-48959. 12376536
Samsonov, V.V., V.V. Samsonov, and S.P. Sineoky. (2002). DcrA and dcrB Escherichia coli genes can control DNA injection by phages specific for BtuB and FhuA receptors. Res. Microbiol. 153: 639-646.
Schalk IJ., Lamont IL. and Cobessi D. (2009). Structure-function relationships in the bifunctional ferrisiderophore FpvA receptor from Pseudomonas aeruginosa. Biometals. 22(4):671-8. 19153809
Schauer, K., B. Gouget, M. Carrière, A. Labigne, and H. de Reuse. (2007). Novel nickel transport mechanism across the bacterial outer membrane energized by the TonB/ExbB/ExbD machinery. Mol. Microbiol. 63: 1054-1068. 17238922
Schryvers, A.B. and I. Stojiljkovic. (1999). Iron acquisition systems in the pathogenic Neisseria. Mol. Microbiol. 32: 1117-1123. 10383753
Shipman, J.A., J.E. Berleman, and A.A. Salyers. (2000). Characterization of four outer membrane proteins involved in binding starch to the cell surface of Bacteroides thetaiotaomicron. J. Bacteriol. 182: 5365-5372. 10986238
Shipman, J.A., K.H. Cho, H.A. Siegel, and A.A. Salyers. (1999). Physiological characterization of SusG, an outer membrane protein essential for starch utilization by Bacteroides thetaiotaomicron. J. Bacteriol. 181: 7206-7211. 10572122
Shultis, D.D., M.D. Purdy, C.N. Banchs, and M.C. Wiener. (2006). Outer membrane active transport: structure of the BtuB:TonB complex. Science 312: 1396-1399. 16741124
Smajs, D. and G.M. Weinstock. (2001). The iron- and temperature-regulated cjrBC genes of Shigella and enteroinvasive Escherichia coli strains code for colicin Js uptake. J. Bacteriol. 183: 3958-3966. 11395459
Udho, E., K.S. Jakes, S.K. Buchanan, K.J. James, X. Jiang, P.E. Klebba, and A. Finkelstein. (2009). Reconstitution of bacterial outer membrane TonB-dependent transporters in planar lipid bilayer membranes. Proc. Natl. Acad. Sci. USA 106: 21990-21995. 19959664
Vanderpool, C.K. and S.K. Armstrong. (2004). Integration of environmental signals controls expression of Bordetella heme utilization genes. J. Bacteriol. 186: 938-948. 14761988
Vianney, A., T.M. Lewin, W.F. Beyer, Jr., J.C. Lazzaroni, R. Portalier, and R.E. Webster. (1994). Membrane topology and mutational analysis of the TolQ protein of Escherichia coli required for the uptake of macromolecules and cell envelope integrity. J. Bacteriol. 176: 822-829. 8300535
Wei, X., L.A. Sayavedra-Soto, and D.J. Arp. (2007). Characterization of the ferrioxamine uptake system of Nitrosomonas europaea. Microbiology. 153: 3963-3972. 18048911
Wexler, H.M., E.K. Read, and T.J. Tomzynski. (2002). Characterization of omp200, a porin gene complex from Bacteroides fragilis: omp121 and omp71, gene sequence, deduced amino acid sequences and predictions of porin structure. Gene 283: 95-105. 11867216
Wolff, N., N. Izadi-Pruneyre, J. Couprie, M. Habeck, J. Linge, W. Rieping, C. Wandersman, M. Nilges, M. Delepierre, and A. Lecroisey. (2008). Comparative analysis of structural and dynamic properties of the loaded and unloaded hemophore HasA: functional implications. J Mol Biol 376: 517-25. 18164722
Yoneyama, H. and T. Nakae. (1996). Protein C (OprC) of the outer membrane of Pseudomonas aeruginosa is a copper-regulated channel protein. Microbiology 142(Pt8): 2137-2144. 8760927