Supramolecular organization of bacterial aerobic respiratory chains: From cells and back

BBABIO-47552; No. of pages: 8; 4C: 2 Biochimica et Biophysica Acta xxx (2015) xxx–xxx

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Supramolecular organization of bacterial aerobic respiratory chains: From cells and back☆ Ana M.P. Melo a,⁎, Miguel Teixeira b a b

Instituto Superior de Agronomia, Universidade de Lisboa, Tapada da Ajuda, 1349-017, Lisboa, Portugal Instituto de Tecnologia Química e Biológica António Xavier, Universidade Nova de Lisboa, Av. da República, 2780-157, Oeiras, Portugal

a r t i c l e

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Article history: Received 10 July 2015 Received in revised form 31 October 2015 Accepted 2 November 2015 Available online xxxx Keywords: Supercomplex Bacteria Respiratory chain Escherichia coli Bacillus subtilis Microbiology

a b s t r a c t Aerobic respiratory chains from all life kingdoms are composed by several complexes that have been deeply characterized in their isolated form. These membranous complexes link the oxidation of reducing substrates to the reduction of molecular oxygen, in a process that conserves energy by ion translocation between both sides of the mitochondrial or prokaryotic cytoplasmatic membranes. In recent years there has been increasing evidence that those complexes are organized as supramolecular structures, the so-called supercomplexes and respirasomes, being available for eukaryotes strong data namely obtained by electron microscopy and single particle analysis. A parallel study has been developed for prokaryotes, based on blue native gels and mass spectrometry analysis, showing that in these more simple unicellular organisms such supercomplexes also exist, involving not only typical aerobic-respiration associated complexes, but also anaerobic-linked enzymes. After a short overview of the data on eukaryotic supercomplexes, we will analyse comprehensively the different types of prokaryotic aerobic respiratory supercomplexes that have been thus far suggested, in both bacteria and archaea. This article is part of a Special Issue entitled Organization and dynamics of bioenergetic systems in bacteria, edited by Prof Conrad Mullineaux. © 2015 Elsevier B.V. All rights reserved.

1. Brief overview of aerobic respiratory chains investigation The aerobic respiratory chain is one of the most relevant pathways in cells, for it makes possible the occurrence of other pathways dependent on energy supply. ATP molecules are the energy currency in the living world, and the most effective one, for the amount of energy conserved in its phosphate bond is just enough to empower enzymatic reactions, contributing to an efficient use of energy by the cell. Other very energetic molecules in the cell, for example NADH and glucose, contain much more energy, and if used would constitute not only a waste, but also its dissipation as heat could seriously jeopardize cells. Driven by this fact, and also by curiosity, research over the respiratory pathway gained emphasis by the second half of the 20th century and never stopped to increase in relevance in understanding the basics of life, but also to explain health and disease, youth and aging. Besides the genius and persistence of researchers, the progresses in this field have been boosted and brake by advances in technology.

☆ This article is part of a Special Issue entitled Organization and dynamics of bioenergetic systems in bacteria, edited by Prof Conrad Mullineaux. ⁎ Corresponding author. E-mail address: [email protected] (A.M.P. Melo).

A brief chronology of a few major steps further into the knowledge of respiratory chains are listed: 1) The spectrophotometric characterization of mitochondria [1] and oxidative phosphorylation states [2] by Chance and Williams, benefiting from the development of the spectrophotometer by Arnold Beckman in 1940 and the Clark oxygen electrode in the fifties; 2) The chemiosmotic [3] and conformational [4] theories of Peter Mitchel and Paul Boyer, respectively, in the late sixties; 3) The 3-D structure of ATP synthase [5], by John Walker, in the nineties, as well as of the other respiratory complexes; 4) The development of the Blue Native Polyacrylamide Gels BN-PAGE technique and its application to the characterization of mitochondrial complexes that led to the identification of respiratory supramolecular structures [6], by Herman Schagger also in the nineties; Improvements in mass spectrometry analysis enabled sequencing of the less abundant and more difficult to ionize membrane proteins, namely liquid chromatography coupled with tandem mass spectrometry (LC-MS/MS), allowing to detail the composition of the complexes visualized in the BN-PAGE; 5) The generation of 3D models from the analyses of such supramolecular structures, by means of electron microscopy and single particle analysis, particularly boosted by Boekema's group already in the 21st century [7]; and finally, 6) The development of electron tomography and its application to mitochondria, to which Terry Frey [8] and Werner Kuhlbrandt [9] greatly contributed. Throughout this evolution, a movement in the object of the study from

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Please cite this article as: A.M.P. Melo, M. Teixeira, Supramolecular organization of bacterial aerobic respiratory chains: From cells and back, Biochim. Biophys. Acta (2015), http://dx.doi.org/10.1016/j.bbabio.2015.11.001

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cells to organelles, to isolated complexes, and back to supramolecular structures, organelles and cells is observed, reflecting the actual need to integrate the innumerous contributions into a global perspective of the oxidative phosphorylation pathway and of this into the cell. 2. Oxidative phosphorylation In both eukaryotic and prokaryotic aerobic worlds, there is a process by which the reducing equivalents, resulting from cell sugar, lipid and amino acid catabolism, are oxidized via a chain of enzymes, the respiratory chain, that culminate in the reduction of oxygen to water. Throughout this chain, some redox reactions are coupled to ion-translocation across the membrane, forming a transmembrane ion-motive force that is used by ATP synthase to synthesize ATP. This process is the socalled oxidative phosphorylation. 2.1. Mammalian mitochondria respiratory chain In detail, and in mammalian mitochondria, the so-called paradigm, the oxidative phosphorylation (OXPHOS) pathway is mainly composed by the NADH:ubiquinone oxidoreductase or complex I, the succinate:ubiquinone oxidoreductase (SQR) or complex II, the bc1 ubiquinol:cytochrome c oxidoreductase or complex III, the aa3 cytochrome c:oxygen oxidoreductase or complex IV, and the ATP synthase also known as complex V (Fig. 1). The flow of electrons between complexes I or II and complex III is mediated by the lipophilic molecule, ubiquinone, and from complex III to complex IV, the electrons pass by the soluble electron carrier cytochrome c, located in the intermembrane space. Proton translocation occurs from the matrix to intermembrane space by complexes I, III and IV, conserving energy in a proton motive force that is used in the synthesis of ATP [10], or in motility and ion transport. 2.2. Diverging from the model Protists, fungi and plant mitochondria have additional enzymes, namely alternative rotenone-insensitive NAD(P)H:quinone oxidoreductases, or type II NAD(P)H dehydrogenases (e.g. [11,12,13]), some of which are sensitive to calcium (e.g. [14]), and alternative oxidases (AOX) (e.g. Arum maculatum [15]).

2.3. OXPHOS organization Three models try to account for the organization of the OXPHOS pathway in the inner membranes of mitochondria or the plasma membranes of prokaryotes. The solid state model based on the knowledge that the transfer of electrons from reducing substrates to oxygen occurred via a sequentially organized cytochrome pathway, that included cytochromes b, c, a and a3, proposes that these enzymes would be tightly packed in a spatial arrangement ensuring substrate accessibility and a high catalytic rate [16]. The random collision model suggested by Hackenbrock and co-workers, aware of the possibility to purify and reconstitute functionally active respiratory chain complexes, postulated the need of multiple collisions to accomplish electron transfer within the respiratory components [17]. In this model, the respiratory enzymes diffuse laterally and independently of each other, occurring multicollisional electron transfer, dependent on the redox components diffusion rate [18]. The more recent plasticity model tries to reconcile the solid state and the random collision models. It suggests a dynamic model where individual complexes and supramolecular organizations comprising sets of different individual complexes coexist, assembling and disassembling on cell demand (e.g. [19]).

2.4. Supramolecular organization of OXPHOS—respiratory supercomplexes Although supramolecular assemblies of respiratory chain enzymes have been identified in all domains of life, based on evidences from multiple technical approaches (see below), the existence of supercomplexes is still a matter of debate, particularly in the prokaryotic world. For instance, kinetic data in yeast mitochondria showed that cytochrome c may be pre-bound to the aa 3 oxygen reductase, but this interaction is determined by the bimolecular interactions between these two proteins and their stoichiometric ratio, rather than by an effective trapping of the soluble carrier within a particular supramolecular structure [20]. This implies that the behavior of this respiratory chain segment is in agreement with the random collision model [[17]]. In fact, supercomplexes have been proposed as a strategy to a better efficiency of the respiratory pathway, not only allowing higher yields of energy conservation, by enabling substrate channeling [21] and enhancing the stability of the respiratory enzymes [22], but also, and due to the former, by minimizing the production of reactive oxygen species [23].

Fig. 1. Mammalian mitochondria electron transfer chain. In dashed boxes the alternative enzymes present in the mitochondria of plants and fungi. I, II, III and IV, NADH:ubiquinone oxidoreductase (complex I), succinate:ubiquinone oxidoreductase (complex II), ubiquinol:cytochrome c oxidoreductase (complex III) and cytochrome c:oxygen oxidoreductase (complex IV), respectively. NDH-2, type II or alternative NADH dehydrogenase, AOX, alternative oxidase. Solid arrows represent the direction of electron flow; dashed arrows for alternative pathways.

Please cite this article as: A.M.P. Melo, M. Teixeira, Supramolecular organization of bacterial aerobic respiratory chains: From cells and back, Biochim. Biophys. Acta (2015), http://dx.doi.org/10.1016/j.bbabio.2015.11.001

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Although the focus of this article is the identification and characterization of aerobic prokaryotic supercomplexes, it is worthy to step into a few examples of their mitochondrial counterparts and their features, as their knowledge represents the state of the art, and a possible way through to push forward research in this segment of the prokaryotic world. 2.4.1. Supercomplex I + III2 + IV1–4—the respirasome1 Mitochondrial respiratory supercomplexes with variable compositions and stoichiometries have been isolated and their structure determined by electron microscopy and single particle analysis. The mitochondrial respirasome, consisting of a NADH:O2 oxidoreductase pathway was identified in animals [24], plants [25] and fungi [26]. Structural investigations of this supramolecular association in bovine mitochondria revealed only a few points of direct contact, between the matrix exposed regions of complexes I, III and IV. In this structure, complex I and one of complex III monomers appear to be linked by the movement of ubiquinol, between its putative binding sites in complex I and in the cytochrome b subunit of the bc1 complex, apparently facing each other and separated by 13 nm. The cytochrome c binding sites of complexes III and IV are in close proximity, 11 nm, allowing the soluble cytochrome c to move between each other, within a short distance. In the respirasome with a I1 + III2 + IV1 stoichiometry, the monomeric complex IV interacts with the second monomer of complex III, where cytochrome b and Rieske Fe–S subunits are in close proximity with complex IV subunits III, VIa and VIIa [24,27]. 2.4.2. The I1–2 + III2 and III2 + IV1–4 supercomplexes Several smaller modules of the respirasome were also described in mammals, plant and fungi, which can be considered as intermediates of the respirasome, consistently with the plasticity model, or the result of harsher solubilization processes and, therefore, devoid of physiologic significance. The ratio of bovine heart respiratory complexes I, III, and IV was calculated as 1:3:6, and a network organization consisting of large and small supercomplexes (I1 + III2 + IV4 and III2 + IV4) in a 2:1 ratio was proposed [28]. Further studies from the same group suggested a “respiratory string”, in which one III2 + IV4 supercomplex connects two [I1 + III2 + IV4]2 respirasomes, the interactions between supercomplexes occurring by their complex IV dimers [29]. A “respiratory string” organization of respiratory supercomplexes was also suggested for potato mitochondria, but in this case it is composed of I2 + III2 + IV2 building blocks, and the interaction between them is mediated by the concave side of each monomeric complex IV, ultimately corresponding to a dimeric structure interface [30]. Similarly to the proposed potato tuber I2 + III2 + IV2 building block, in the Saccharomyces cerevisiae III2 + IV2 supercomplex, complex IV is attached to complex III2 as a monomer in two opposite sides, leaving its concave side available for protein-protein interactions [31]. 2.4.3. Other examples Complex II containing supercomplexes are hardly detectable in BNPAGE. Nevertheless, this enzyme was also described as part of respiratory hetero-oligomerizations, namely of a supercomplex that further contains complexes I, III and IV identified in mouse fibroblasts [32]. Moreover, it was suggested to interact with complexes III and IV in S. cerevisiae [33]. AOX was shown to form supercomplexes with complex III in tomato and amoeba [34]. Furthermore it was identified as part of I1 + IV1 and IV2 supercomplexes, in Neurospora crassa mutants devoid of complex III [35]. FOF1 ATP synthase was detected in the form of dimers and larger homo-oligomers in mitochondria from mammals [36], plants [37] and 1

The subscript indicates the stoichiometry of each complex.

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fungi [38]. The detection of tetrameric, hexameric, and octameric FOF1ATP synthases suggested that these oligomers are assembled from dimeric building blocks to form long ribbons [39]. ATP synthase oligomerization and cristae morphogenesis were suggested to be tightly related based on experiments in yeast mutants lacking the e- and g-subunits of ATP synthase, where the oligomerization of this enzyme does not occur. In these mutants, the membrane looks extended and organized in a number of separate vesicles, with few or no cristae [40,41]. 2.4.4. Special features of mitochondrial supercomplexes 2.4.4.1. Physiological role. The supramolecular organization of respiratory chains is proposed to optimize oxidative phosphorylation, namely by allowing substrate channeling, individual complexes stability [22], and tight regulation of reactive oxygen species (ROS) production [23]. Accordingly, membrane components of eukaryotes are often organized in small domains of variable composition and length scale – microcompartments – contributing to facilitate the diffusion of electron transfer substrates and to prevent energy losses as proton leakage [42]. Noteworthy, FOF1-ATP synthase oligomeric structures are localized along highly curved cristae ridges with respiratory chain supercomplexes in the adjacent regions [43]. It was proposed that the shape of cristae influences supercomplex formation and stability [44]. Nonetheless, it seems more likely that, based on electron cryo-tomography, subtomogram averaging, and electron crystallographic image processing evidences from bovine mitochondria, it is the dimeric ATP synthase supercomplex that imposes the formation of mitochondrial cristae [9]. Metabolic control analysis of NADH oxidation in bovine heart submitochondrial particles determined high flux control coefficients for complexes I and III, suggesting that these enzymes work as “single enzyme units” with channeling of ubiquinol [45]. Substrate channeling of ubiquinone was further supported by the structural analysis of the bovine respirasome that predicted short distances between the ubiquinone binding sites of complexes I and III (see above). In addition, the confinement of mobile electron carriers such as quinones and cytochrome c within the supercomplex facilitates the transfer of electrons between the individual enzymes and precludes the loss of intermediates that if randomly diffused could contribute to the formation of harmful ROS. In contrast with harsh solubilized mammalian mitochondria, under mild solubilization conditions, the activity of complex I monomers is not detected in BN-PAGE, corroborating the role of respiratory supercomplexes in the stabilization of the individual enzymes [46,47]. In fact, only 14–16% of total bovine mitochondrial complex I, and 10% of the human enzyme, was found in the free form after digitonin solubilization [28,48], suggesting its structural stabilization by complexes III and IV in mammalian mitochondria [49]. In agreement, primary genetic assembly defects of human mitochondrial complex III led to secondary loss of complex I and prevented respirasome formation [50]. More recently, and based on flux control analysis of bovine heart mitochondria, it was suggested that supercomplexes evolved as a strategy to maintain an extremely high protein concentration and, simultaneously, avoid nucleation and aggregation. The authors further suggest that the observed supercomplexes are weak and transient associations that only become “fixed” when the membrane is partially disrupted [51]. Such argument is based on the absence of known supercomplex-mediating factors in the available structural data on isolated complexes III and IV, the lack of strong contact points in the I + III2 + IV supercomplex [24], and the fact that supercomplexes are only preserved when using mild detergents, such as digitonin. 2.4.4.2. A key lipid. With few exceptions, cardiolipin is a minor phospholipid component found in the inner mitochondrial membrane and also in most bacterial and archaeal membranes. It has been found bound to several mitochondrial and bacterial proteins in their crystal forms,

Please cite this article as: A.M.P. Melo, M. Teixeira, Supramolecular organization of bacterial aerobic respiratory chains: From cells and back, Biochim. Biophys. Acta (2015), http://dx.doi.org/10.1016/j.bbabio.2015.11.001

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typically sitting at monomer interfaces of oligomeric assemblies and appearing to mediate the contact between two monomers or the contact between the protein surface and the bilayer [52]. Cardiolipin was also suggested to play a functional and structural role in mitochondrial respiratory chain supercomplexes, the supercomplex III2 + IV2 of S. cerevisiae being almost totally dissociated in a mutant strain devoid of cardiolipin [53], and the concentration of supercomplexes I1 + III2 and I1 + III2 + IV1 being severely decreased in Barth syndrome patients, whose mitochondrial cardiolipin content is low [54]. In accordance, the gaps at the interface of the complexes of the mammalian I1 + III2 + IV1 respirasome may be occupied by cardiolipin molecules [24]. In bacteria, to date, there is no evidence of cardiolipin importance for supercomplex assembly. In fact, there was no difference in supercomplex composition between an E. coli strain devoid of cardiolipin synthase and the wild type organism, as deduced from BN-PAGE in gel activities of digitonin solubilized membranes (Melo et al. unpublished data). 2.4.4.3. Relationship with other mitochondrial proteins. Proteins other than oxidative phosphorylation enzymes have been suggested to play an important role in supercomplex assembly and or stability. In S. cerevisiae, respiratory supercomplex factors Rcf1 and Rcf2, members of the conserved hypoxia-induced gene 1 (Hig1) protein family, were identified as components of III2 + IV1 and III2 + IV2 supercomplexes, respectively [55]. In addition, Hig2A, the mammalian homolog of Rcf1, is also part of the mammalian III2 + IV1 supercomplex. In its absence, the content of supercomplexes comprising complex IV is severely decreased [56]. In S. cerevisiae, the ADP/ATP carrier was described to be associated with the III2 + IV2 supercomplex [57]. Several enzymes of the fatty acid β-oxidation complex, specifically the acyl-CoA dehydrogenases, were identified in the respirasome of rat liver mitochondria, showing evidence of direct electron transfer to the respiratory chain [58]. 3. General features of aerobic respiratory chains in prokaryotes In prokaryotic cells, the aerobic respiratory pathways are located in the cytoplasmic membrane. The cellular organization varies among bacteria and archaea. In Gram-negative bacteria, a single peptidoglycan layer stays between the cytosolic membrane and the outer membrane. In contrast, in Gram-positives, several peptidoglycan layers are located in the outer surface of the cytoplasmic membrane. Archaea contain in general a single membrane, surrounded mainly by surface layer

proteins (S-layers), but some archaea may have multiple polymers, such as the polysaccharide pseudomurein or methanochondroitin, or even two membranes [59,60,61]. The prokaryotic respiratory chains are very flexible pathways that contain minimal functional units of mitochondrial enzymes, i.e., with a much lower number of subunits containing the catalytic centers, and may have several alternative complexes, for example, multiple oxygen reductases. The composition of these complexes varies in accordance with environmental conditions, like oxygen and substrate availability (Fig. 2). The organization of prokaryotic aerobic respiratory chains is similar to that of mitochondria. There is an entry point for electrons, a dehydrogenase that accomplishes their transfer to a quinone. In turn, electrons are transferred to oxygen via a quinol:electron carrier oxidoreductase and an oxygen reductase, or directly by a quinol:oxygen oxidoreductase (Fig. 2). In bacteria, NADH:, succinate: and formate:quinone oxidoreductases are the most commonly observed dehydrogenases. NDH-1 is a multimeric membrane enzyme, composed by 13 or 14 different subunits, that couples the redox reaction of NADH oxidation and reduction of quinones to ion translocation across the inner membrane, most frequently protons [13]. NDH-2 are soluble single polypeptides that attach membrane surfaces via amphipatic helices; several cases of NDH-2 homo-dimers are described [62]. NDH-3 or Na+-NQR, are frequently found in the respiratory chains of pathogenic bacteria. These are also multimeric membranous enzymes, a functional analogue of NDH-1 that translocates sodium concomitantly with the NADH:quinone oxidoreductase reaction [63]. Different organisms, in response to environmental conditions, synthesize several types of quinones, lipid soluble electron carriers, which, beyond the electron transfer systems, have a role in gene and oxidative stress regulation [64,65]. In fact, the structural diversity presented by quinone molecules, linked with different physical and functional characteristics, like reduction potentials, polarity, steric and interaction constrains, have proved useful for bacterial taxonomy [66]. Quinone molecules can be grouped into three major groups, according to their structural features: benzothiophenquinones, benzoquinones and naphtoquinones. In turn, benzothioquinones can be divided in caldariellaquinones, sulfolobus quinones and tricyclicquinones; benzoquinones in plastoquinones and ubiquinones; and naphtoquinones in menaquinones, thermoplasmaquinones and phylloquinones. Different quinones types may coexist in the same

Fig. 2. Model of prokaryotic aerobic respiratory chains. Dashed or solid lines across the respiratory complexes indicate alternative electron pathways. Dashed arrows from the inner to the outer surface of the cytosolic membrane indicate eventual ion translocation by the respiratory complexes. “+” on top of vertical arrows refers to translocated proton or sodium ions. “+” and “−” refer to positive and negative charges on the outer and inner leaflets of the cytosolic membrane, respectively.

Please cite this article as: A.M.P. Melo, M. Teixeira, Supramolecular organization of bacterial aerobic respiratory chains: From cells and back, Biochim. Biophys. Acta (2015), http://dx.doi.org/10.1016/j.bbabio.2015.11.001

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prokaryote, being differentially synthesized according to the growth conditions (see [67] for a review). Two examples in Bacteria and Archaea are i) the ability of Escherichia coli to produce ubiquinone or menaquinone, [68], and ii) and the presence of three benzothiophenquinones, caldariella quinone, sulfolobus quinone, and the tricyclic quinone, in Sulfolobus acidocaldarius and S. solfataricus [69]. Downstream quinones, the simplest respiratory chains contain solely a quinol:oxygen reductase that may translocate protons, like the heme copper enzymes cytochromes bo3 or aa3, or not, like cytochrome bd, or the alternative oxidase AOX. Nonetheless, cytochrome bd is electrogenic [70]. There are also respiratory chains more similar to mitochondria, comprising a cytochrome bc1 oxidoreductase or analogue complex that receives electrons from quinol to reduce a soluble electron carrier as cytochrome c (e.g. [71]), or the high potential iron–sulfur protein (HiPIP) (e.g. [72,73]). In turn, the reduced electron carrier will reduce oxygen via proton-translocating heme-copper oxygen reductases of A, B, or C types [74]. Heme-copper enzymes are often named according to the types of hemes they contain, e.g., aa3, caa3, cbb3 and ba3. Several organisms contain multiple types of heme copper reductases. Bacterial FOF1 ATP synthase couples the energy of the ion-motive force, conserved from the electron transfer reactions, to the phosphorylation of ADP into ATP. In contrast with mitochondrial ATP synthases, the bacterial counterparts have not been described as dimers, maybe in agreement with the straight shape of the cytoplasmic membrane. 4. Supramolecular organization of respiratory chains from prokaryotes In prokaryotes, several different aerobic respiratory supercomplexes were reported in archaea and both in Gram-negative and Gram-positive bacteria. Such diversity is an argument that supports these supramolecular assemblies as a physiological strategy to improve the efficiency of the respiratory pathways. 4.1. Quinol:electron-carrier:oxygen reductases: the most widespread supercomplexes Homologues or analogues of the mitochondrial III–IV supercomplex were reported in all domains of life. The widespread nature of these supercomplexes suggests that it may be crucial for a tight regulation of the respiratory chain cytochrome pathway. The archaea aerobic respiratory chains containing the complexes SoxABCD and SoxM are analogous to the mitochondrial cytochrome pathway. SoxC subunit is an analog of complex III cytochrome b, but with type a hemes, and SoxA and SoxB resemble subunits II and I of heme-copper oxygen oxidoreductases. In S. acidocaldarius, the genes encoding SoxABC form a single operon [75]. The SoxM supercomplex comprises six subunits (SoxEFGHIM) organized in two functional subcomplexes, related to mitochondrial complexes III and IV. The complex III analog subcomplex is composed of subunits SoxF and SoxG, a homolog of the Rieske Fe–S protein subunit assembling also a binuclear [Fe–S] centre, and a structural analog of complex III cytochrome b subunit that, similarly to SoxABCD, comprises two a-type hemes. Subcomplex SoxM–SoxH has two hemes b (b and b3), a CuB centre and a binuclear CuA centre, and belong to the type A heme-copper oxygen reductases [76,77]. The copper protein sulfocyanin (SoxE subunit) completes this electron transfer pathway, sitting between the subcomplexes. SoxABCD and SoxM resemble the mitochondrial III–IV supercomplexes and catalyse quinol:oxygen oxidoreductase activity, mediated by sulfocyanin. They were identified in the respiratory chains of S. acidocaldarius and S. tokodai strain 7 [75,76,78]. In bacteria, supercomplexes of this kind were reported in Gram negatives and Gram positives. The first example of a bc1:caa3 supercomplex in a Gram-positive bacterium was described in Bacillus PS3 [79], when

Fig. 3. Distribution of identified aerobic supercomplexes among prokaryotes. ACIII, alternative complex III, FDH-O, oxygen expressed formate dehydrogenase, NAR, nitrate reductase, SDH, succinate dehydrogenase, SQR, sulfide:quinone oxidoreductase, Rcy, Rusticyanin.

the use of BN- and CN-PAGE and milder detergents was not yet foreseen (Fig. 3). A 1:1 stoichiometry was proposed based on cross-linking experiments [80]. In Mycobacterium smegmatis [81] and Corynebacterium glutanicum [82] respiratory chains, oligomerizations of the bcc complex (analogue to the Bacillus subtilis bc complex) and cytochrome aa3 oxygen reductase were reported. Recently, a hybrid respiratory supercomplex consisting of M. tuberculosis cytochrome bcc and M. smegmatis cytochrome aa3 was isolated [83] (Fig. 3). In B. subtilis, a bc:caa3 megacomplex was described with a stoichiometry of [(bc)2(caa3)4]2. Additionally, two other sub-oligomerizations were retrieved, a (bc)4:(caa3)2 and (bc)2:(caa3)4 supercomplexes, that consist of the building blocks forming the megacomplex [84]. A stringlike organization was previously hypothesized for plant, mammalian and fungi mitochondria [29,30,31], but this was the first time it was observed in prokaryotes. Oca and coworkers [85], using lysozyme treatment instead of French press to obtain cell disruption, have also identified a bc:caa3 supercomplex in this bacterium. In contrast to Sousa et al. [84], these authors identified cytochrome c550 in the supercomplex. Nevertheless, considering that subunit II of B. subtilis caa3 oxygen reductase has an additional covalently bound cytochrome c, it is possible that electron transfer in this supercomplex is independent of a soluble cytochrome c [86]. The bc 1 :aa 3 supercomplex of the Gram-negative Paracoccus denitrificans was also isolated with cytochrome c 552 [82,87,88]. Additionally, in this bacterium, a I 1 + III 4 + IV 4 supercomplex, the so-called respirasome, was identified [87,88] (Fig. 3). Finally, quinol:electron carrier:oxygen reductases supercomplexes were also described in other bacteria (Fig. 3). In the thermohalophilic bacterium Rhodothermus marinus, a supercomplex of an alternative complex III and caa3 oxygen reductase was isolated [89]. In Bradyrhizobium japonicum a bc1:cbb3 supercomplex was reported [90]. A peculiar

Please cite this article as: A.M.P. Melo, M. Teixeira, Supramolecular organization of bacterial aerobic respiratory chains: From cells and back, Biochim. Biophys. Acta (2015), http://dx.doi.org/10.1016/j.bbabio.2015.11.001

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respirasome with iron oxidase and oxygen reductase activities, composed by a bc complex, a cytochrome c (Cyc1), (Cyc2) and an aa3 oxygen reductase, was described in Acidithiobacillus ferrooxidans [91], linking iron oxidation to oxygen reduction in this iron-oxidizing bacterium. Another unconventional respirasome-like supercomplex, containing a sulfide:quinone oxidoreductase, a dimeric bc1 complex and a cytochrome ba3 oxygen reductase, was retrieved from Aquifex aeolicus [92, 93].

4.2. Respirasome-like supercomplexes The respirasome concept emerged in mitochondria, upon the identification of full sets of respiratory chain complexes assembled in a supercomplex, namely the already mentioned NADH:O2 oxidoreductase respirasome in mitochondria of several eukaryotes (see above). These, thus, correspond to fully functional segments of respiratory chains, from the electrons entry point to an oxygen reductase. As such, and since bacterial aerobic respiratory chains are more versatile with regard to its components, analogous structures are present also in bacteria. This evidence suggests that not only the respirasome enables a more efficient respiratory process, but also that the observed smaller supercomplexes may be actors of a supercomplex biogenesis pathway [48], although the possibility that these are only artifacts from the solubilization processes should not be discarded. With the exception of a yet poorly characterized SDH:aa3 supercomplex, of the respiratory chain of B. subtilis [85], evidences of supercomplexes involving quinol:oxygen oxidoreductases were only described for the respiratory chain of E. coli. Until recently, it was generally accepted that respiratory supercomplexes were absent from this bacterium. In turn, it was proposed that there would be specialized patches with respiratory enzymes within the cytoplasmic membrane called respirazones [94]. Melo and co-workers have recently detected several homo and hetero-oligomerizations of E. coli respiratory enzymes, namely, a formate:oxygen oxidoreductase (FdOx), composed by the formate dehydrogenase (Fdo) and cytochromes bo3 and bdI, in a 1:1:1 stoichiometry [95,96], and a succinate:oxygen oxidoreductase of unknown stoichiometry, that included SQR and cytochrome bdII [97], based on the analyses of digitonin-solubilized membranes from wild type and respiratory mutants by BN-PAGE, sucrose gradients, and LC/MS-MS. In vivo studies of individual respiratory complexes tagged with fluorescent probes and monitored through fluorescence microscopy approaches were performed to tackle the question of their co-localization, but no evidences were found [98]. In addition, Erhardt and coworkers [99] reported mobile and immobile fluorescent patches of respiratory supercomplexes in E. coli, larger than individual complexes, consistent with previous observations of dimers of cytochrome bo3 [95,100] and trimers of SQR [95,101]. Pairs of formate dehydrogenase and oxygen reductases, SQR and oxygen reductases and NDH-1 and NDH-2 that were not assayed yet, could corroborate in vivo the presence of the supramolecular structures already identified in vitro in E. coli. Comprehensive multi-level analysis of the E. coli respiratory chain that also included growth dynamics, gene expression and enzyme activity [96], using principal component analysis, established positive correlation between the formate:oxygen oxidoreductase (FdOx) activity and the transcription of the genes encoding cytochromes bo3 and bdI, further supporting the findings associating these complexes in the FdOx supercomplex. The presence of two different oxygen reductases in this supercomplex may ensure its activity in a wide range of oxygen concentrations, given the different affinities of cytochromes bo3 and bdI towards oxygen. The KM of the formate:oxygen oxidoreductase reaction, determined in E. coli membranes respiring formate, is 170 ± 20 μM [96], within the range of FDH-N KM (120 μM) [102]. FdOx was the first respirasome reported in E. coli, and the first evidence of an

oxygen-terminated respiratory pathway involving the aerobic formate dehydrogenase (FDH-O). 4.3. Other aerobic respiratory supercomplexes A NADH oxidoreductase supercomplex, composed by NDH-1 and NDH-2 in a stochiometry of 1:1 was also identified in the respiratory chain of E. coli [95]. A comprehensive multi-level analysis of the E. coli respiratory chain, using Kendall rank correlations pointed a positive correlation between the transcription of NDH-1, NDH-2 and cytochrome bdI encoding genes [97], suggesting that cytochrome bdI could be associated to this supercomplex. However, and in spite of the fact that NADH:O2 oxidoreductase activity inhibited by KCN is produced by the NDH-1:NDH-2 band excised from the BN-PAGE, neither the size nor the mass spectrometry analysis was conclusive in this respect. It could be that the oxygen reductase is lost during the solubilization procedures. Considering that NDH-1 is not observed in a BN-PAGE of digitonin-solubilized membranes from a strain devoid of NDH-2, it is possible that the presence of this enzyme is crucial for the assembly of an intact complex I in E. coli [95]. Noteworthy, saturation transfer electron paramagnetic resonance and differential scanning calorimetry assays demonstrated direct interaction between cytochrome caa3 and F1 F0 -ATP synthase in the alkaliphilic Bacillus pseudofirmus OF4, being tempting to speculate the existence of a supercomplex of these enzymes [103] (Fig. 3). In fact, a supercomplex formed by cytochrome aa3 and F1-ATPase was also suggested in B. subtilis [85]. 4.4. An anaerobic supercomplex of unexpected partners An interesting complex was identified in the membranes of B. subtilis growing aerobically, involving a nitrate reductase (NAR) and a succinate oxidoreductase [84,85]. This supramolecular organization, with 2:1 stoichiometry, was unexpected and is the first evidence of a respiratory pathway linking the oxidation of succinate to the reduction of nitrate. It challenges the conventional strict association of SQR to aerobic respiration, associating it to an enzyme that is part of anaerobic respiration. Succinate oxidation mediated by menaquinone-dependent SQRs implicates the transfer of two electrons to menaquinone in an endergonic process [104,105], due to the higher reduction potential of succinate/ fumarate when compared to the menaquinone/menaquinol pair. This could be bypassed by NAR within the supercomplex, by the uptake of two protons from the inner wall zone to the binding site of menaquinone [106]. It is noteworthy that, in B. subtilis respiratory chain nitrate pairs with oxygen as a favorite terminal electron acceptor. Anaerobic respiratory chain supercomplexes from Archaea have also been reported. A hydrogen-oxidizing, and sulfur-reducing supramolecular assembly was described in the membranes of A. aeolicus [107], Acidianus ambivalens [108] and Pyrodictium abyssi [109]. 5. Final remarks In summary, in recent years several respiratory supercomplexes have been identified in bacteria and archaea, paralleling the betterstudied respirasomes from eukaryotic mitochondria. This suggests that the supercomplexes may be a general feature in the three kingdoms of life, leading to a more efficient management of energy conservation. Nevertheless, in prokaryotes more solid evidences, like by microscopy, are still lacking, namely due to the low amounts of each supercomplex that have been isolated. But it should be stressed again that the catalytic relevance of supercomplexes has been recently questioned, namely by kinetic studies based on the electron carriers ubiquinol and cytochrome c, in mitochondria. Clearly, more studies are needed to settle the in vivo importance of respiratory supercomplexes and their role in biological energy conservation.

Please cite this article as: A.M.P. Melo, M. Teixeira, Supramolecular organization of bacterial aerobic respiratory chains: From cells and back, Biochim. Biophys. Acta (2015), http://dx.doi.org/10.1016/j.bbabio.2015.11.001

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Please cite this article as: A.M.P. Melo, M. Teixeira, Supramolecular organization of bacterial aerobic respiratory chains: From cells and back, Biochim. Biophys. Acta (2015), http://dx.doi.org/10.1016/j.bbabio.2015.11.001