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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 Å 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 many 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 Å from its high-affinity site in HasA into a site of lower affinity in HasR is coupled with the exergonic  formation of the 2 protein complex. 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 suggested that OprC forms small channels after the precursor 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 #1.B.14.2.3) is one example of such a system, while the TbpAB (TC #1.B.14.2.12) and the LbpAB (TC #1.B.14.2.4) systems are two other examples. The LbpB and TbpB lipoproteins are homologous, but the smaller HpuA lipoprotein is not demonstrably homologous to either LbpB or 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 M. 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 entry route of the bacteriocin, pesticin.

Wolff et al. (2007) reported the 3-D NMR structure of apoHasA (TC# 1.A.14.5.1) 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 Å, of loop L1 bearing H32. Comparison of loaded and unloaded HasA dynamics on different time scales revealed 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.14.1.2) 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)

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