Anaerobiosis versus Aerobiosis inEscherichia coli

Like most bacteria,Escherichia coli has a flexible and branched respiratory chain that enables the prokaryote to live under a variety of environmental conditions, from highly aerobic to completely anaerobic.E. coli induces the expression of those respiratory components that are best suited to a particular environment. In general, the bacterial respiratory chain is composed of dehydrogenases, a quinone pool, and reductases. Substrate-specific dehydrogenases transfer reducing equivalents from various donor substrates (NADH, succinate,α-glycerophosphate, formate, hydrogen, pyruvate, and lactate) to a quinone pool (menaquinone, ubiquinone, and dimethylmenoquinone). Then electrons from reduced quinones (quinols) are transferred by terminal reductases to different electron acceptors. Under aerobic growth conditions, the terminal electron acceptor is molecular oxygen. A transfer of electrons from quinol to O₂ is served by two major oxidoreductases (oxidases), cytochromebo₃ and cytochromebd (it is worth noting that accumulated evidence over the past few years also suggests the contribution of a secondbd-type oxidase, cytochromebd-II, to the electron transfer and membrane potential generation). When oxygen is not available (under anaerobic conditions), alternative terminal electron acceptors, including nitrate, nitrite, dimethyl sulfoxide, trimethylamineN-oxide, and fumarate, can be used, and the reaction is catalyzed by nitrate reductases, nitrite reductase, dimethyl sulfoxide reductases, trimethylamineN-oxide reductase, and fumarate reductase, respectively (reviewed in references1 and2).

Two Types of Quinol Oxidases Only

Terminal oxidases of aerobic respiratory chains of bacteria, which use O₂ as the final electron acceptor, can oxidize one of two alternative electron donors, either cytochromec or quinol. Oxidases utilizing cytochromec are called cytochromec oxidases, whereas oxidases oxidizing quinol are referred to as quinol oxidases (3,4,5,6,7,8,9,10,11,12,13). Cytochromec oxidases cannot directly accept reducing equivalents from quinol. For this purpose, there is an additional, middle component of the respiratory chain between dehydrogenase and oxidase, the cytochromebc₁ complex, which enables the transfer of electrons from quinol to cytochromec. Respiratory chains of many aerobic bacteria, such asParacoccus denitrificans andAzotobacter vinelandii, contain thebc₁ complex and both types of terminal oxidase, cytochromec and quinol oxidases. For instance,P. denitrificans has one quinol oxidase (ba₃) and two cytochromec oxidases (aa₃ andcbb₃) (14,15).A. vinelandii has two quinol oxidases (bo₃ andbd) and one cytochromec oxidase (cbb₃) (reviewed in references16 and17). As shown inFig. 1, the aerobic respiratory chain ofE. coli is much simpler than those ofP. denitrificans andA. vinelandii. It lacks the cytochromebc₁ complex and any cytochromec oxidase but contains instead three quinol oxidases,bo₃,bd, andbd-II (reviewed in references17,18,19,20, and21).

Physiological Functions

Cytochromebo₃ predominates under high aeration, whereas cytochromebd is expressed under low oxygen tension (22,23,24) (Table 1). It is of interest that the cytochromebo₃ level increases about 150-fold during aerobic growth, but the cytochromebd level falls only 3-fold, i.e., the change in the cytochromebd level in response to oxygen is much smaller than that of the cytochromebo₃ level (23). Both oxidases catalyze the oxidation of ubiquinol-8 to allow cellular respiration with oxygen as the terminal electron acceptor (25). Cytochromebd can also oxidize menaquinol-8 (26,27), which replaces ubiquinol-8 upon a change of growth conditions from aerobic to anaerobic (2).

Both cytochromebo₃ and cytochromebd are primary generators of a transmembrane gradient of electrochemical H⁺ potentials (Δμ_H⁺), because the reaction arising from the transfer of reducing equivalents from quinol to O₂ is coupled directly to transmembrane charge separation (28,29,32,50,51,52,53,54). The energy conserved in the form of Δμ_H⁺ can be used by theE. coli cell for ATP synthesis, the transport of nutrients, and other useful work. Thus, the main function of both oxidases is energy conservation. The two enzymes, however, are different in their bioenergetic efficiencies (transmembrane proton translocation ratios, or the number of protons delivered to the periplasmic side of the membrane per electron [H⁺/e⁻ ratios]), with an H⁺/e⁻ ratio of 2 for cytochromebo₃ and an H⁺/e⁻ ratio of 1 for cytochromebd (28,29) (Table 1). This difference is because cytochromebo₃ is a true proton pump, whereas cytochromebd is not capable of proton pumping (28,29). As sources of oxidizing power, cytochromebo₃ and cytochromebd can support disulfide bond formation upon protein folding catalyzed by the DsbA-DsbB system (55).

Apart from energy conservation, cytochromebd endowsE. coli with a number of specific physiological functions. Cytochromebd can serve as an oxygen scavenger and inhibit the degradation of O₂-sensitive enzymes present under anaerobic and microaerophilic conditions (56). In a recent systematic mutational analysis to elucidate the contribution of the respiratory pathways to the abilities of commensal and pathogenic (enterohemorrhagic)E. coli strains to colonize a streptomycin-treated mouse intestine, mutants lacking cytochromebd failed to colonize whereas cytochromebo₃ was found not to be necessary for colonization (57).

The cytochromebd contents increase not only at low oxygen concentrations, but also under some unfavorable conditions, such as alkaline pH (58), high temperature (59,60), the presence of uncouplers-protonophores (58,61,62), and low concentrations of cyanide (63) in growth media. Mutants defective in cytochromebd are sensitive to H₂O₂ (60) and a self-produced extracellular factor that inhibits their growth (64,65). Mutants that cannot synthesize cytochromebd are also unable to exit from the stationary phase and resume aerobic growth at 37°C (66,67). The expression of cytochromebd, instead of cytochromebo₃, may enhance bacterial tolerance to oxidative and nitrosative stresses (68,69,70,71). In particular, cytochromebd contributes to bacterial resistance to peroxynitrite (71,72), nitric oxide (68,69,70,71,73,74,75,76,77), carbon monoxide (78,79), and hydrogen peroxide (59,70,71,80,81,82,83,84,85,86).

Inhibitors

Table 2 compares the effects of different inhibitors on the respiratory activities of cytochromebo₃ and cytochromebd inE. coli. Inhibitors of the quinol oxidases can be divided into two groups: quinol-like compounds acting at a quinol-binding site(s) and heme ligands (e.g., cyanide, azide, and NO) acting at the oxygen-binding/reducing site. A specific feature of cytochromebd is that it is much less sensitive to cyanide and azide than cytochromebo₃ (32) (Table 2). The lower sensitivity of cytochromebd to anionic heme ligands may be a result of an elevated electron density on the central ion of iron due to the breaking of the circle conjugate π-electron structure in thed-type porphyrin ring and/or may point to a more hydrophobic environment for the O₂-reducing site of cytochromebd than for that of cytochromebo₃. It is of interest that the quinolone-type compound aurachin D and its derivatives in submicromolar concentrations specifically inhibit cytochromebd but virtually do not affect cytochromebo₃ (87). These outcomes may indicate some differences in the specific structures of quinol-binding sites in cytochromebo₃ and cytochromebd. It has been shown recently that cytochromebd inE. coli is a bacterial membrane target for a cationic cyclic decapeptide, gramicidin S (50% inhibitory concentration, ∼5.3μM) (Table 2), although it has been generally accepted that the main target of gramicidin S is the membrane lipid bilayer rather than the protein components (88). This finding can provide new insight for the molecular design and development of novel gramicidin S-based antibiotics. The effect of gramicidin S on cytochromebd and some other membrane-bound proteins may be the alteration of the protein structure through binding to the hydrophobic protein surface (88).

Oxidase Encoding

Regulation of Gene Expression

Under high oxygen tension,E. coli expresses cytochromebo₃ (encoded bycyoABCDE), whereas cytochromebd (encoded bycydABX) is moderately repressed (22,23,24). The expression of thecyoABCDE andcydABX operons is controlled by the two global transcriptional regulators Arc and Fnr (2,23,120,121,122,123,124,125,126). Arc is a two-component regulatory system that includes ArcA, a cytosolic response regulator, and ArcB, a transmembrane histidine kinase sensor. ArcA controls several hundred genes (127) and responds to the oxidation state of the quinone pool, which is sensed by ArcB (128). ArcB is activated in the course of the transition from aerobic to microaerobic growth and remains active during anaerobic growth. Upon stimulation, ArcB autophosphorylates and then transphosphorylates ArcA (128,129). Under microaerobic conditions (i.e., oxygen tension of 2 to 15% of air saturation), the increased level of phosphorylated ArcA represses thecyoABCDE operon and activates thecydABX operon (130).

Another global regulator, Fnr (an oxygen-labile transcription factor regulating hundreds of genes), controls the induction of anaerobic processes inE. coli (131,132). The Fnr protein has an Fe-S cluster which serves as a redox sensor. The levels of the Fnr protein are similar under both aerobic and anaerobic conditions (122,133), but the protein is active only during anaerobic growth. The active Fnr protein represses bothcyoABCDE andcydABX operons during a transition to anaerobic conditions (i.e., oxygen tension of less than 2% of air saturation) (124,125,133).

Quinones

Quinones are lipophilic molecules dissolved within the lipid bilayer of the cytoplasmic membrane. TheE. coli membrane contains three types of quinones that all have an octaprenyl side chain (C₄₀). These are a benzoquinone, ubiquinone, and two naphthoquinones, menaquinone and dimethylmenaquinone. Both cytochromebo₃ and cytochromebd catalyze the two-electron oxidation of ubiquinol-8 to ubiquinone-8 (Fig. 2) (apparent midpoint redox potential [E_m] = +110 mV [2]), coupled to the four-electron reduction of O₂ to 2H₂O (E_m = +820 mV). Cytochromebd can also oxidize menaquinol-8 to menaquinone-8 (Fig. 2) (E_m = −80 mV [2]) (26,27). Ubiquinone-8 is predominant during aerobic growth but is replaced by menaquinone-8 upon the transition from aerobiosis to anaerobiosis (2,134,135). It was shown previously that cytochromebo₃ contains a tightly bound ubiquinone (136). The presence or absence of bound quinone in solubilized cytochromebd depends on the purification protocol (20). In some preparations of purified cytochromebd, there is no quinone (32,47,51,137), whereas others clearly contain bound quinone (52,54,138).

Cytochromebo₃ Prosthetic Groups

Cytochromebo₃ contains three redox-active metal groups: a low-spin hemeb, which is involved in quinol oxidation, hemeo₃, and Cu_B; the latter two groups compose a binuclear center, which is the site of the binding of O₂ and its reduction to water. The chemical cofactors are hemeb, corresponding to protoporphyrin IX (protoheme, or hemeB); hemeo₃, corresponding to the protoheme with a long farnesyl side chain attached (hemeO); and the Cu_B center, represented by the Cu atom ligated by three histidine residues. In the three-dimensional (3D) structure of cytochromebo₃, all prosthetic groups were found to be within subunit I (139). In addition to the metal centers, there is also one tightly bound ubiquinone cofactor. Although the X-ray structure did not show any bound quinone in the crystallized enzyme, the site-directed mutagenesis studies identified residues that modulate the properties of the bound quinone (140,141,142).

Cytochromebd Prosthetic Groups

Cytochromebd is composed of three subunits, I (CydA), II (CydB), and III (CydX), which are typical integral membrane proteins. The subunits carry three metal-containing redox centers, such as two protoheme IX groups (hemesb₅₅₈ andb₅₉₅) and a chlorin molecule (hemed) (Fig. 3), which are proposed to be in 1:1:1 stoichiometry per the enzyme complex, but no copper ion (157,158,159,160,161). Hemeb₅₅₈ appears to be located within subunit I. Subunits I and II are required for the assembly of hemeb₅₉₅ and hemed, suggesting that these two hemes may reside at the subunit interface (112). Both hemeb₅₅₈ and hemed are presumed to be oriented with their heme planes perpendicular to the membrane plane. Hemeb₅₉₅ is possibly oriented with its heme plane at ∼55° with respect to the plane of the membrane (162).

Redox Potentials of Hemes in Cytochromebd

The E_m values of hemesb₅₅₈,b₅₉₅, andd in theE. coli cytochromebd solubilized inn-dodecyl-β-d-maltoside at pH 7.0 are +176, +168, and +258 mV, respectively (49) (Table 1). Similar values were reported for cytochromebd contained in bacterial membranes (158,159,197), reconstituted in liposomes (198), or solubilized in Tween 20 or Triton X-100, in which the enzyme is active (198). Notably, the E_m value of hemeb₅₅₈ can depend on the detergent used for solubilization (198). In particular, octylglucoside and cholate cause a large decrease in the E_m value of hemeb₅₅₈ that also correlates with the reversible inactivation of the enzyme (198). The E_m values of all three heme components of cytochromebd are sensitive to pH values between 5.8 and 8.3, with dependence of −61 mV per pH unit for hemed and −40 mV per pH unit for hemesb₅₅₈ andb₅₉₅, indicating that the reduction of thebd complex is accompanied by enzyme protonation (198). The spectroelectrochemical redox titration and spectral modeling show the strong redox interaction between hemeb₅₅₈ and hemeb₅₉₅, while the interaction between hemed and either hemesb is insignificant (168). Of interest, in the absence of hemed the interaction potential between hemeb₅₅₈ and hemeb₅₉₅ is much larger compared with the situation when hemed is present (168).

3D Structure ofbo₃ Oxidase

The 3D structure of thebo₃ oxidase fromE. coli at 3.5-Å resolution was reported in 2000 (139). The structure confirms that the overall architecture of this complex is very similar to those of all other members of the heme-copper oxidase superfamily. The whole integral protein contains 25 transmembrane helices, of which subunit I has 15, subunit II has only 2, subunit III has 5, and subunit IV has 3 helices. All known enzyme cofactors were found in subunit I. The transmembrane helices of this subunit are not perpendicular to the membrane plane but are tilted about 20 to 35° against it. When viewed from the top (P side), they are arranged in an anticlockwise direction and form three semicircular arcs, organized in a quasithreefold axis of symmetry. Three pores are formed in the center of the arcs. One pore houses the binuclear center (hemeo₃ and Cu_B) of the oxidase and includes the proton-conductive K channel directed from the binuclear center toward the N (negative) side of the membrane. Another pore retains hemeb; the last pore is devoid of cofactors but is used for the proton-conductive D channel.

Hemeb is located at a depth of about one-third of the membrane thickness from the P side and oriented perpendicular to the membrane plane, such that its propionates are pointing toward the P side of the membrane (Fig. 4). The hemeo₃ is located at the same depth as hemeb, the plane of hemeo₃ is also perpendicular to the membrane, and the propionates point toward the P side in a manner similar to hemea. Hemeb and hemeo₃ are facing each other at an angle of 104 to 108^o. At an ∼5-Å distance from the iron of hemeo₃, a copper atom designated Cu_B is located. In addition to this Cu atom that is coordinated by the three histidines, there is another important structure identified in all heme-copper oxidases and represented by the covalently bound H284_I and Y288. The three histidines and the tyrosine form a conjugated π-electron system around the Cu_B center. Cytochromebo₃ has been proposed to have two ubiquinone-binding sites, one with high (Q_H) and one with low (Q_L) affinity for ubiquinone (136). It has also been postulated that electrons are transferred from the Q_L site to hemeb via the ubiquinone bound at the Q_H site. Site-directed mutagenesis studies (140,142) have identified residues that modulate the properties of the Q_H site. The model of a Q_H quinone-binding site including R71, D75, H98, and Q101 residues is also supported by the results of X-ray crystallography (139).

The protein medium itself cannot facilitate proton delivery toward the binuclear center or across the membrane, and in order to overcome this limitation, the oxidase has special proton-conductive structures. It is proposed that these structures are based on chains of hydrogen bonds between hydrogen-bonding protein side groups (polar and/or protonatable) and water molecules, whereby the proton is transferred via a Grotthuss type mechanism. At least two proton-conductive channels have been identified primarily by site-directed mutagenesis (199,200,201), and these findings were later confirmed by X-ray crystallography (139). One of them is the so-called K pathway, named after the highly conserved lysine 362 (199,200), which is situated approximately halfway through the channel (Fig. 4). This pathway starts with S315 and S299 and continues through conserved residues K362_I and T359_I toward the hydroxyethyl farnesyl side chain of hemeo₃ and Y288_I in the proximity of the binuclear center. The other channel is named D after the highly conserved D135_I (201,202), which is situated near the surface of the enzyme on the N side. D135_I, together with T211_I, forms a mouth that leads via polar residues N124_I, N142_I, S145_I, T149_I, T201_I, and T204_I to E286_I (Fig. 4), which is an important residue for the proton-pumping mechanism.

Proposed Structure of Cytochromebd

To date, the X-ray structure of cytochromebd is not available; however, the findings from conventional studies of the protein topology in the membrane suggest that all three hemes are located near the periplasmic side of the membrane (176,177).Figure 5 shows topological models of subunits I (CydA) and II (CydB) of cytochromebd fromE. coli (27). Both subunits are integral membrane proteins showing no sequence homology to the subunits of the heme-copper oxidase superfamily (e.g., cytochromebo₃). Subunit I consists of nine transmembrane helices, with the N terminus in the periplasm and the C terminus in the cytoplasm (176). Subunit II is composed of eight transmembrane helices, with both N and C termini in the cytoplasm (176). Newly discovered subunit III, the 37 amino acid CydX protein (42,43,109), is proposed to consist of the only membrane-spanning helix, with the N terminus in the cytoplasm and the C terminus in the periplasm (21,80,109). Subunit I contains a large hydrophilic domain, which is called the Q-loop, connecting transmembrane helices VI and VII. As shown by many experimental approaches, the Q-loop is involved in quinol binding and oxidation (163,164,165,166,203,204). Thus, the quinol-oxidizing site in cytochromebd is located on the periplasmic side of the membrane. It is worth mentioning that the size of the Q-loop is taken into account to categorize the bacterial cytochromesbd (20,172).

Based on 815 sequences of the cytochromebd gene available, it was possible to search for highly conserved residues in the corresponding protein (27). It was shown previously that subunit II evolved significantly faster than subunit I, with the result that subunit II exhibits greater sequence diversity (205). A number of residues in subunit I are totally (>99%) conserved in the 815 sequences (27). These residues include H19 (the hemeb₅₉₅ axial ligand [180]), H186 and M393 (the hemeb₅₅₈ axial ligands [173,174,175]), K252 and E257 (involved in quinol binding [204]), R448 (having an unknown function), and E99, E107, and S140 (proposed to be components of a proton channel [54,176] and important for binding in the hemed-hemeb₅₉₅ diheme site [27,137]). Slightly less conserved (95 to 99%) are E445 (required for charge compensation at the hemeb₅₉₅-hemed oxygen-reducing site upon the full reduction of oxygen by two electrons [52]), N148 (a plausible component of a proton channel), and R9 (having an unknown function) (27). Somewhat less conserved (∼85%) are R391 (which stabilizes the reduced form of hemeb₅₅₈ [206]) and D239 (having an unknown function); however, these residues are totally conserved within the group of cytochromesbd with a long Q-loop, to which theE. coli enzyme belongs (27). Other conserved residues are glycines, prolines, phenylalanines, and tryptophans, which may play structural roles. There is only one totally (>99%) conserved residue (W57) in subunit II (27). Residues R100, D29, and D120 of subunit II are totally conserved within the family of long-Q-loop cytochromebd, and the residue at position 58 in subunit II (according to the numbering for theE. coli enzyme) is either an aspartate or a glutamate. The N-terminal portion of subunit II is thought to be involved in the binding of hemed and hemeb₅₉₅ (27,207).

A multiple sequence alignment of 299 homologues of the newly found CydX subunit reveals the conserved amino acid motif that includes the residues Y3, W6, G9, and E/D25 (109). Of these residues, the first three are part of the predicted transmembrane α-helix being localized to the same side of the helix (109). The latter suggests that this is possibly the side of the α-helix of CydX that interacts with the other subunits in cytochromebd (109).

Since the active site of O₂ reduction is located near the periplasmic surface and protons for H₂O production are taken from the bacterial cytoplasm, there must be at least one transmembrane proton-conducting pathway to convey protons from the cytoplasm to the hemeb₅₉₅-hemed site (51,52,54,176) (Fig. 6).

Ligand Binding to the Cytochromebo₃ Binuclear Center

Ligands that bind to the binuclear center of cytochromebo₃ can be divided into two classes: uncharged molecules like CO and NO, which preferably bind to the binuclear center in the reduced form and induce the transition of the high-spin heme to the low-spin state, making it six coordinate, and ionizable molecules, like HCN and NaN₃, or formate, which preferably bind to the oxidized heme. The binding of the second group of ligands can result in a different spin state for hemeo₃. Some of the ligands can bind either to hemeo₃ only or to a site between the two metals forming the binuclear center. The dynamics of ligand exchange can be used to characterize the possible dynamics of the binding of the substrate and the partial products of the reaction generated during the catalytic cycle.

Ligand Binding to Cytochromebd

Since hemesd andb₅₉₅ in cytochromebd are in the high-spin pentacoordinate state, these redox centers can potentially bind ligands. It has to be expected that the reduced form of thebd enzyme can bind mainly electroneutral molecules like O₂, CO, and NO and that the oxidized cytochromebd binds ligands in the anionic form, such as cyanide and azide. It appears that hemed binds ligands readily but that the ligand reactivity of hemeb₅₉₅ is minor (170,184,189). It was reported previously that hemeb₅₅₈, although a low-spin hexacoordinate, may also bind ligands (e.g., CO and cyanide) to some extent (170,189). Such marginal reactivity is due possibly to the weakening of the bond of the methionine axial ligand (M393) with the hemeb₅₅₈ iron caused by the isolation procedure and/or protein denaturation (189).

Mechanism of Cytochromebo₃ Functioning

Cytochromebo₃ catalyzes the final step ofE. coli respiration—the oxidation of ubiquinol-8 and the reduction of molecular oxygen. The reduction of one dioxygen molecule to water requires four electrons, which are supplied by two molecules of ubiquinol on the P side, and four protons, taken up from the N side of the membrane. The reduction of oxygen to water is an exergonic process, coupled with the release of large amounts of energy. This energy is conserved in the form of Δμ_H⁺. The formation of Δμ_H⁺ by cytochromebo₃ is based on two principles: vectorial chemistry and proton pumping. Since the protons and electrons for oxygen reduction to water are taken from different sides of the membrane, the reduction results in the net transfer of four charges across the membrane. At the same time, the enzyme is able not only to catalyze the oxygen reduction, but also to utilize the released energy for proton pumping. This process was discovered in 1977 (239) by the demonstration that the reduction of molecular oxygen to water by mitochondrial cytochromec oxidase is linked to the pumping of additional four protons across the membrane dielectric (239). Later, such functional ability was shown for cytochromebo₃ (240). Hence, the overall reaction catalyzed by cytochromebo₃ can be described by the following equation:

where Q is ubiquinone, QH₂ is ubiquinol, H⁺_N is proton taken from the N side of the membrane (the cytosol), and H⁺_P is proton released to the P side of the membrane (the periplasmic space). The mechanism coupling electron transfer reactions with the transmembrane proton translocation is still under debate. Let’s look through the main elements of this mechanism.

Mechanism of Cytochromebd Functioning

Under physiological conditions, cytochromebd can oxidize ubiquinol-8 and menaquinol-8.In vitro, thebd enzyme can also utilize shorter-chained ubiquinols, menadiol, duroquinol, and artificial electron donors such asN,N,N′,N′-tetramethyl-p-phenylendiamine (TMPD) (in the presence of excess ascorbate). Of thein vitro substrates, ubiquinol-1 (plus excess dithiothreitol) shows the highest turnover numbers (34,198). The apparentK_m values for some reductants are shown inTable 1. As noted above, the activity of the purifiedbd enzyme strongly depends on the nature of the detergent in which the enzyme is solubilized. Cytochromebd is inactive in octylglucoside or cholate but shows high activity in Tween 20 or Triton X-100 (198) orN-lauroyl-sarcosine (73). The ubiquinol-1 oxidase activity of cytochromebd has a broad optimum above pH 7.5 but decreases at more acidic pH values (198). Cytochromebd possesses three distinct active sites—for quinol oxidation, TMPD oxidation, and oxygen reduction. All three sites seem to be located at or close to the periplasmic surface of the membrane. Electrons donated from quinol transfer to hemeb₅₅₈ and then to theb₅₉₅-d diheme site, whereas electrons donated from TMPD transfer directly to theb₅₉₅-d site, bypassing the quinol-binding site and hemeb₅₅₈ (165).

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