Many quinone-reactive enzyme complexes that are part of membrane-integral eukaryotic or prokaryotic respiratory electron transport chains contain one or more haem b molecules embedded in the membrane. In recent years, various novel proteins have emerged that are devoid of haem b but are thought to fulfil a similar function in bacterial anaerobic respiratory systems. These proteins are encoded by genes organized in various genomic arrangements and are thought to form widespread membrane-bound quinone-reactive electron transport modules that exchange electrons with redox partner proteins located at the outer side of the cytoplasmic membrane. Prototypic representatives are the multihaem c-type cytochromes NapC, NrfH and TorC (NapC/NrfH family), the putative iron–sulfur protein NapH and representatives of the NrfD/PsrC family. Members of these protein families vary in the number of their predicted transmembrane segments and, consequently, diverse quinone-binding sites are expected. Only a few of these enzymes have been isolated and characterized biochemically and high-resolution structures are limited. This mini-review briefly summarizes predicted and experimentally demonstrated properties of the proteins in question and discusses their role in electron transport and bioenergetics of anaerobic respiration.

Introduction

Membranous quinone-reactive b-type cytochromes are key components of multi-subunit complexes serving in aerobic and anaerobic respiratory electron transport chains of both eukaryotic and prokaryotic organisms. Prominent examples are the cytochrome bc1 complex, cytochrome bo3 and cytochrome bd quinol oxidases as well as quinone-reactive membrane-bound complexes of Ni/Fe-hydrogenase, formate dehydrogenase, nitrate reductase, succinate dehydrogenase and fumarate reductase. The haem b groups of these enzymes are located within the membrane plane, usually axially ligated by histidine side chains deriving from at least two different transmembrane helical regions. Furthermore, haem b is often involved in the composition of catalytic centres operative in quinone/quinol turnover. In many cases, electron transport via these proteins is coupled with the generation of a protonmotive force across the membrane by either proton pumping, or the Q-cycle or the redox loop mechanism. In recent years, however, an ever-growing number of haem b-independent, quinone-reactive proteins have been identified in bacteria that contain either haem c or iron–sulfur centres or that are, apparently, devoid of any prosthetic groups. These proteins are encoded in a variety of different contexts in bacterial genomes, thus forming versatile electron transport modules that interact with suitable redox partner proteins catalysing redox reactions in bacterial respiration (see Table 1 for a compilation). The aim of the present mini-review is to provide a brief overview of the function of such protein families, focusing on the available biochemical and structural information.

Table 1
Hydroquinone-reactive protein families and exemplary family members discussed in the present study

Fe/S, iron–sulfur centre; Mo-bis-MGD, molybdenum bound to bis-molybdopterin guanine dinucleotide; TMAO, trimethylamine N-oxide.

Family Protein Genetic context Cofactor content* Redox partner (cofactor)† Reference(s) 
NapC/NrfH      
 NapC Periplasmic nitrate reductase Four haem c (exp., P. denitrificans, P. pantotrophus, E. coliNapB (two haem c) or possibly NapM (four haem c[2,9,10,32,33
 NrfH Cytochrome c nitrite reductase Four haem c (exp., W. succinogenes, D. vulgarisComplex formation with NrfA (five haem c[36,8
 NirT Cytochrome cd1 nitrite reductase Four haem c (pred., Ps. stutzeriNirS (haems c and d1[34
 CymA None Four haem c (pred., Shewanella spp.) Various (see text) [11,1315
 Cyt. cM552 Hydroxylamine oxidoreductase Four haem c (pred., N. europaeaCyt. c554 (four haem c[12
 FccC Methacrylate reductase Four haem c (pred., W. succinogenesFccAB (flavocytochrome c[35
 TorC TMAO reductase Five haem c (exp., E. coliTorA (Fe/S, Mo-bis-MGD) [7
 DorC DMSO reductase Five haem c (exp., R. capsulatusDorA (Fe/S, Mo-bis-MGD) [36
NapH      
 NapH Periplasmic nitrate reductase Two Fe/S clusters (pred.), possible metal binding via two CX3CP motifs (E. coli, W. succinogenesNapG (Fe/S) [16,18,19
 NosH N2O reductase See NapH (W. succinogenesNosG (Fe/S) [20
 NosR N2O reductase See NapH, contains an additional N-terminal flavin-binding domain (exp., Ps. stutzeriNot known [22,23
NrfD/PsrC      
 NrfD Cytochrome c nitrite reductase Not known (E. coliNrfC (Fe/S) [26
 PsrC Polysulfide reductase Bound MM (exp., W. succinogenesComplex formation with PsrB (Fe/S) and PsrA (Fe/S, Mo-bis-MGD) [28,29
 TtrC Tetrathionate reductase Not known (Salmonella entericaPutative complex formation with TtrB (Fe/S) and TtrA (Fe/S, Mo-bis-MGD) [37
 MccD mcc gene cluster Not known (W. succinogenesMccC (Fe/S) [31
Family Protein Genetic context Cofactor content* Redox partner (cofactor)† Reference(s) 
NapC/NrfH      
 NapC Periplasmic nitrate reductase Four haem c (exp., P. denitrificans, P. pantotrophus, E. coliNapB (two haem c) or possibly NapM (four haem c[2,9,10,32,33
 NrfH Cytochrome c nitrite reductase Four haem c (exp., W. succinogenes, D. vulgarisComplex formation with NrfA (five haem c[36,8
 NirT Cytochrome cd1 nitrite reductase Four haem c (pred., Ps. stutzeriNirS (haems c and d1[34
 CymA None Four haem c (pred., Shewanella spp.) Various (see text) [11,1315
 Cyt. cM552 Hydroxylamine oxidoreductase Four haem c (pred., N. europaeaCyt. c554 (four haem c[12
 FccC Methacrylate reductase Four haem c (pred., W. succinogenesFccAB (flavocytochrome c[35
 TorC TMAO reductase Five haem c (exp., E. coliTorA (Fe/S, Mo-bis-MGD) [7
 DorC DMSO reductase Five haem c (exp., R. capsulatusDorA (Fe/S, Mo-bis-MGD) [36
NapH      
 NapH Periplasmic nitrate reductase Two Fe/S clusters (pred.), possible metal binding via two CX3CP motifs (E. coli, W. succinogenesNapG (Fe/S) [16,18,19
 NosH N2O reductase See NapH (W. succinogenesNosG (Fe/S) [20
 NosR N2O reductase See NapH, contains an additional N-terminal flavin-binding domain (exp., Ps. stutzeriNot known [22,23
NrfD/PsrC      
 NrfD Cytochrome c nitrite reductase Not known (E. coliNrfC (Fe/S) [26
 PsrC Polysulfide reductase Bound MM (exp., W. succinogenesComplex formation with PsrB (Fe/S) and PsrA (Fe/S, Mo-bis-MGD) [28,29
 TtrC Tetrathionate reductase Not known (Salmonella entericaPutative complex formation with TtrB (Fe/S) and TtrA (Fe/S, Mo-bis-MGD) [37
 MccD mcc gene cluster Not known (W. succinogenesMccC (Fe/S) [31
*

The cofactor content is either predicted (pred.) from the primary structure or experimentally proven (exp.). In the latter case, the organism(s) from which the protein is derived has been given in the Table; otherwise exemplar organisms are stated.

In those cases where a stable membrane-bound complex is not formed, the interaction of the quinone-reactive protein with the indicated redox partner has not been shown experimentally.

The NapC/NrfH c-type cytochrome family

The NapC and NrfH proteins are related tetrahaem c-type cytochromes consisting of approx. 175 amino acid residues that are assumed to form an N-terminal membrane-spanning helix and a globular cytochrome c domain situated at the outside of the bacterial membrane (Table 1; Figures 1A and 1B) [1]. They form a protein family that was previously referred to as the NapC/NirT family since NirT from Pseudomonas stutzeri was the first such protein to which a function had been assigned (in this case electron transport to periplasmic cytochrome cd1 nitrite reductase). NapC and NrfH donate electrons, either directly or indirectly, to periplasmic nitrate reductase (NapA) and periplasmic cytochrome c nitrite reductase (NrfA) respectively (Table 1). The prototypic NapC from Escherichia coli has been shown to be involved in electron transport from both ubiquinol and menaquinol to NapA [2], whereas NrfH from Wolinella succinogenes or Desulfovibrio vulgaris anchors a menaquinol-reactive complex with NrfA in the membrane [36]. In both cases, multihaem c-type cytochromes act as redox partner proteins (Table 1). Thus it is not surprising that a subfamily exists to which a monohaem cytochrome c domain is fused at the C-terminus (Table 1; Figure 1C). An example is the TorC protein from E. coli that donates electrons to the periplasmic TorA [7].

Quinone-reactive proteins and their redox partners

Figure 1
Quinone-reactive proteins and their redox partners

Schematic architecture and cofactor content of members of the NapC/NrfH (AC), NapH (D) and NrfD/PsrC (E, F) families and their role in bacterial electron transport. Quinone-reactive proteins are shown in grey and redox partner proteins in white. For simplicity, quinol oxidation, electron transfer and substrate reduction are shown non-stoichiometrically. The diamonds and cubes depict haem c groups and [4Fe-4S] centres respectively. Broken arrows indicate that the side of the membrane to which protons are liberated is speculative. Sec and Tat (twin-arginine translocation) refer to the translocation system used for protein transport across the cytoplasmic membrane. The illustration of NrfH is adopted from the D. vulgaris NrfH crystal structure [6]. The – and + signs denote the inside and outside of the cytoplasmic membrane respectively. Mo, molybdenum bound to bis-molybdopterin guanine dinucleotide; Nt, the N-terminus of the quinone-reactive protein, MMb, bound methyl-menaquinone; MMbH, hydroquinone anion of MMb.

Figure 1
Quinone-reactive proteins and their redox partners

Schematic architecture and cofactor content of members of the NapC/NrfH (AC), NapH (D) and NrfD/PsrC (E, F) families and their role in bacterial electron transport. Quinone-reactive proteins are shown in grey and redox partner proteins in white. For simplicity, quinol oxidation, electron transfer and substrate reduction are shown non-stoichiometrically. The diamonds and cubes depict haem c groups and [4Fe-4S] centres respectively. Broken arrows indicate that the side of the membrane to which protons are liberated is speculative. Sec and Tat (twin-arginine translocation) refer to the translocation system used for protein transport across the cytoplasmic membrane. The illustration of NrfH is adopted from the D. vulgaris NrfH crystal structure [6]. The – and + signs denote the inside and outside of the cytoplasmic membrane respectively. Mo, molybdenum bound to bis-molybdopterin guanine dinucleotide; Nt, the N-terminus of the quinone-reactive protein, MMb, bound methyl-menaquinone; MMbH, hydroquinone anion of MMb.

The crystal structure of NrfH from D. vulgaris was solved as part of a quinol-oxidizing (NrfHA2)2 complex [6]. A putative menaquinol-binding site was proposed at the periplasmic side of the membrane, situated in the vicinity of haem 1, that serves as an entrance to a densely packed electron-transferring haem c wire. The identity of the proposed menaquinol oxidation site is supported by experiments using variants of W. succinogenes NrfH [1,8]. Curiously, two haems of D. vulgaris NrfH deviate from the common bis-histidine axial haem ligation pattern found in many c-type cytochromes functional in anaerobic respiration [6]. Haem 1 is proximally ligated by a methionine residue arranged in a CX2CHXM haem c-binding motif, whereas haem 4 shows histidine/lysine ligation, with the lysine ligand provided by an NrfA subunit. In contrast, spectroscopic characterization of NapC from either Paracoccus denitrificans or Paracoccus pantotrophus indicated bis-histidine ligation of each haem c group [9,10], a feature that was also described for purified CymA from Shewanella frigidimarina [11]. Hence, the presence of different haem c ligation patterns in NapC- and NrfH-type proteins is quite likely, and this suggestion is supported by primary structure alignments [1].

Other members of the NapC/NrfH family are cytochrome cM552 from Nitrosomonas europaea, which serves in electron transport from hydroxylamine to the quinone pool during nitrification, and CymA from Shewanella oneidensis for which a promiscuous role in anaerobic respiration with either fumarate, Fe(III), Mn(IV), nitrate, nitrite or DMSO has been shown (Table 1) [1214]. Furthermore, CymA of Shewanella sp. strain ANA-3 was reported to be required for arsenate respiration [15].

With the exception of NrfH, the family members listed in Table 1 do not form stable complexes with their respective redox partners. Protein-protein interaction has been shown for TorC and TorA from E. coli as well as for CymA and the periplasmic flavocytochrome c fumarate reductase from S. oneidensis MR-1 [7,14]. The latter protein as well as P. pantotrophus NapC were functional in electron transport even in the absence of the N-terminal hydrophobic region. This is in line with the assumption that a hydrophobic patch situated in the vicinity of the quinol-binding site enables close contact with the membrane [10,14].

The NapH-type quinol dehydrogenase

In addition to NapC, various nap gene clusters contain the genes napH and napG whose products have been predicted to form a membrane-bound quinol dehydrogenase complex (Table 1; Figure 1D). NapH proteins contain four hydrophobic segments that are likely to form transmembrane domains, two conserved CX3CP signatures and two four-cysteine clusters typically involved in [4Fe-4S] centre formation. The predicted topology has been confirmed experimentally for E. coli NapH, implying that all four polycysteine motifs are located at the cytoplasmic side of the membrane (Figure 1D) [16]. NapG is a putative poly-ferredoxin that probably binds four [4Fe-4S] centres. Formation of a complex between NapH and periplasmic NapG has been shown for W. succinogenes, which performs NapC-independent nitrate respiration, in contrast with E. coli [17,18]. Characterization of E. coli mutants that form either ubiquinone or menaquinone indicated that the putative NapGH complex functions as a ubiquinol dehydrogenase that transfers electrons via NapC to NapAB, whereas menaquinol oxidation was carried out by NapC independently of NapGH [2]. In contrast, NapGH is a probable menaquinol dehydrogenase complex in W. succinogenes whose subunits have both been shown to be essential for nitrate respiration [19]. The architecture and localization of the quinone-reactive site in NapH is not known and it cannot be excluded that more than one such site is present. It has been speculated that NapGH is involved in the generation of a protonmotive force during electron transport from the quinol pool to NapA, but there is no clear experimental evidence to support this hypothesis [2]. In this respect, it will be highly interesting to elucidate the function of the cytoplasmic, potentially metal-binding CX3CP motifs as well as of the [4Fe-4S] centres of NapH. These could play a role in transmembrane electron transfer, redox sensing/balancing and/or enzyme maturation, for example in reductive activation of a Nap system component.

In W. succinogenes, homologues of NapH and NapG were identified in the nos gene cluster encoding cytochrome c N2O reductase (cNosZ) [20], a feature that seems to be common in ϵ-proteobacteria [21]. While all typical properties of NapH are conserved in NosH, the spacing of the polycysteine clusters in NapG and NosG is slightly different. This might mean that the NapG/NosG proteins act as specific adaptors that facilitate electron transfer from the quinol dehydrogenase NapH/NosH to the suitable redox partner in either the Nap or Nos system. NosH has recently been shown to interact with NapG, and the resulting complex was found to be functional in W. succinogenes nitrate respiration [18].

Notably, the arrangement of the four polycysteine motifs of NapH/NosH is also present in various other proteins, for example in NosR, which is encoded in nos gene clusters outside the ϵ-proteobacteria (Table 1) [22]. NosR contains an additional N-terminal periplasmic flavin-binding domain that was found to be essential for N2O respiration in Ps. stutzeri [23]. The phenotype of an NosR-deficient Ps. stutzeri mutant is in line with an essential role for NosR in electron transport to NosZ, and modification of the polycysteine motifs affected the N2O-reducing activity of intact cells [23]. Other NapH-type proteins are encoded by mauN, rdxA and ccoG/fixG/rdxB present in methylotrophs (methylamine dehydrogenase gene cluster) and photosynthetic and aerobic bacteria (cytochrome cbb3 oxidase accessory gene cluster) respectively. The function of these proteins is essentially unknown (see [24,25] for more details).

The NrfD/PsrC family of integral membrane proteins

NrfD is a polytopic membrane protein encoded in the nrf gene cluster of enteric bacteria lacking nrfH (Table 1 and Figure 1E). NrfD was shown to be essential for formate-dependent nitrite reduction of E. coli [26] and was predicted to traverse the membrane eight times, with both the N- and C-termini located in the periplasm. According to the model presented in Figure 1(E), NrfD forms a complex with NrfC, which is predicted to bind four [4Fe-4S] clusters, and this complex catalyses electron transfer via the pentahaem cytochrome c NrfB to NrfA [27]. Such an electron transfer pathway is envisaged to functionally replace the NrfHA complex present in proteobacteria such as W. succinogenes and D. vulgaris (see above). NrfD was proposed to be the most likely candidate to catalyse quinol oxidation in the E. coli Nrf pathway [24], but neither NrfD nor NrfC has been purified, and it is not known whether or not NrfD contains any cofactors.

The assumed NrfDC-type quinol dehydrogenase module is widespread in bacterial anaerobic electron transport chains with homologous proteins present, for example in polysulfide and tetrathionate reductase systems (Table 1). The NrfD homologue PsrC was shown experimentally to form a complex with PsrA and PsrB in the membrane-bound Psr complex of W. succinogenes (Figure 1F) [28,29]. PsrC is the sole membrane anchor of the complex and the two hydrophilic subunits PsrA and PsrB are oriented towards the periplasm. Proteoliposomes containing purified PsrABC as well as the membrane-bound Ni/Fe hydrogenase complex HydABC (anchored in the membrane by the dihaem cytochrome b membrane anchor HydC [30]) did catalyse polysulfide respiration, provided that MM (methyl-menaquinone-6) was present [29]. According to the model of the mechanism of W. succinogenes polysulfide respiration, MM binds to PsrC at an as yet unknown (but most likely to be periplasmically oriented) site and mediates electron transfer within a HydABC/PsrABC supercomplex [28,29]. Electron transport was found to be coupled with protonmotive force generation with a likely H+/e ratio of 0.5 [28]. Site-directed modification of PsrC identified several residues essential for polysulfide respiration that are located in one of the eight predicted hydrophobic helices [29], and it will be interesting to assess their possible role in electron transfer, quinol oxidation and/or transmembrane proton movement with the help of a future crystal structure of an NrfD/PsrC-like protein.

Genes encoding members of the NrfD/PsrC family are found in a variety of different genetic contexts, usually in combination with a gene encoding a polyferredoxin similar to NrfC/PsrB. One such example is the W. succinogenes mcc gene cluster where a complex between MccD and MccC might function in electron transport from menaquinol to the octahaem cytochrome c MccA (Table 1) [31].

Conclusions and outlook

It is intriguing that members of the comparatively small number of cytochrome b-independent quinone-reactive protein families discussed in the present paper serve in otherwise unrelated bacterial respiratory electron transport chains. On the other hand, different modules are employed in electron transport chains that eventually transfer electrons to highly homologous terminal reductases, e.g. NapC and NapH (to NapA) or NrfH and NrfD (to NrfA). In those cases where a stable complex with an appropriate redox partner protein is not formed, the use of such modules has probably been advantageous during evolution due to interchangeability of module-encoding genes in suitable genetic contexts. Furthermore, such modules possibly allow electron exchange with different redox partners, resulting in electron transfer networks that, for example, could serve in redox balancing in the periplasmic space of proteobacteria. Conversely, the formation of stables complexes such as NrfHA and PsrABC ensures that electrons from the quinol pool cannot divert into other respiratory systems. More biochemical and structural information is required to draw a more conclusive picture of the structure and function of the quinone-reactive proteins discussed here. In this context, it will be interesting to examine further the protein–protein interactions and to determine corresponding Kd values that, in principle, could be rate-limiting in electron transfer. Apart from NrfH, the number, location and architecture of quinone-binding sites await clarification, a topic that is of fundamental interest for the bioenergetics of the respiratory systems presented in this paper. So far, there is no experimental evidence contradicting the view that proton exchange during quinone/quinol turnover is limited to the periplasmic side of the membrane, implying non-electrogenic reaction mechanisms. However, proton translocation accomplished by either proton pumping or a quinone cycle cannot be excluded in the case of polytopic membrane proteins such as NapH and NrfD/PsrC. In the future, the proper evaluation of the rapidly growing genetic information will possibly allow reconstruction of the functional evolution of these modules and their role in distinct or branched bacterial electron transport chains. Already, there are some examples of corresponding genes present in the genomes of non-proteobacterial species.

Note added in proof (received 31 July 2008)

It has recently been published that CymA from S. oneidensis, as well as E. coli NapC, are able to function as ferric reductases in E. coli provided that water-soluble forms of reduced iron were supplied [38]. Furthermore, purified cytochrome cM552 from N. europaea was characterized as a tetrahaem cytochrome c ubiquinone reductase exhibiting a 1:3 ratio of high-spin and low-spin haem groups [39]. The location of the predicted menaquinol-binding site of D. vulgaris NrfH was confirmed by determining the crystal structure with bound HQNO (2-heptyl-4-hydroxyquinoline-N-oxide) [40].

The crystal structure of the membrane anchor PsrC of the Thermus thermophilus polysulfide reductase complex PsrABC provided the first structural model for a protein of the NrfD/PsrC family [41]. As predicted in Figure 1(F), PsrC forms eight transmembrane helices and was found to contain a single quinol-binding site at the periplasmic membrane surface. Interestingly, the eight helices are organized in two four-helix bundles, and the first of those carries the quinol-binding site in close proximity to an iron–sulfur centre of PsrB. Apart from the different orientation of the transmembrane helices and the additional cysteine-containing motifs in NapH, PsrB and the N-terminal half of PsrC resemble the model of the NapGH complex shown in Figure 1(D)

Integration of Structures, Spectroscopies and Mechanisms: Second Joint German/British Bioenergetics Conference, a Biochemical Society Focused Meeting held at University of Edinburgh, U.K., 2–4 April 2008. Organized by Ulrich Brandt (Frankfurt, Germany), Steve Chapman (Edinburgh, U.K.), Peter Heathcoate (Queen Mary, University of London, U.K.), John Ingledew (St Andrews, U.K.), Mike Jones (Bristol, U.K.), Bernd Ludwig (Frankfurt, Germany), Fraser MacMillan (University of East Anglia, Norwich, U.K.), Hartmut Michel (Max-Planck-Institute for Biophysics, Frankfurt am Main, Germany), Peter Rich (University College London, U.K.) and John Walker (MRC Dunn Human Nutrition Unit, Cambridge, U.K.). Edited by Ulrich Brandt and Peter Rich.

Abbreviations

     
  • MM

    methyl-menaquinone-6

J.S. is grateful to his co-workers, past and present, whose names are cited in the reference list. Work in our laboratory is supported by the Deutsche Forschungsgemeinschaft (Heisenberg Programme and SFB 472). We thank David J. Richardson (University of East Anglia, Norwich, U.K.) for helpful discussions and comments and Monica Sänger for editing this paper pre-submission.

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