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Biochimica Et Biophysica Acta 1817 (2012) 898–910

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Biochimica Et Biophysica Acta 1817 (2012) 898–910 View metadata, citation and similar papers at core.ac.uk brought to you by CORE provided by Elsevier - Publisher Connector Biochimica et Biophysica Acta 1817 (2012) 898–910 Contents lists available at SciVerse ScienceDirect Biochimica et Biophysica Acta journal homepage: www.elsevier.com/locate/bbabio Review ☆ Biogenesis of cbb3-type cytochrome c oxidase in Rhodobacter capsulatus Seda Ekici a,1, Grzegorz Pawlik b,1, Eva Lohmeyer b, Hans-Georg Koch b,⁎, Fevzi Daldal a,⁎⁎ a University of Pennsylvania, Department of Biology, Philadelphia, PA 19104, USA b Albert-Ludwigs University of Freiburg, Institute of Biochemistry and Molecular Biology, ZBMZ, Freiburg, 79110 Germany article info abstract Article history: The cbb3-type cytochrome c oxidases (cbb3-Cox) constitute the second most abundant cytochrome c oxidase Received 24 September 2011 (Cox) group after the mitochondrial-like aa3-type Cox. They are present in bacteria only, and are considered Accepted 31 October 2011 to represent a primordial innovation in the domain of Eubacteria due to their phylogenetic distribution and Available online 4 November 2011 their similarity to nitric oxide (NO) reductases. They are crucial for the onset of many anaerobic biological processes, such as anoxygenic photosynthesis or nitrogen fixation. In addition, they are prevalent in many Keywords: pathogenic bacteria, and important for colonizing low oxygen tissues. Studies related to cbb3-Cox provide a cbb3-type cytochrome c oxidase Co- or post-translational cofactor insertion fascinating paradigm for the biogenesis of sophisticated oligomeric membrane proteins. Complex subunit Assembly of membrane proteins maturation and assembly machineries, producing the c-type cytochromes and the binuclear heme b3-CuB Copper acquisition center, have to be coordinated precisely both temporally and spatially to yield a functional cbb3-Cox enzyme. Photosynthesis and respiration In this review we summarize our current knowledge on the structure, regulation and assembly of cbb3-Cox, Energy transduction and provide a highly tentative model for cbb3-Cox assembly and formation of its heme b3-CuB binuclear center. This article is part of a Special Issue entitled: Biogenesis/Assembly of Respiratory Enzyme Complexes. © 2011 Elsevier B.V. All rights reserved. 1. Introduction (i. e., cytochrome c oxidase, Cox) and those that use a quinol (i. e., quinol oxidase, Qox). Cox are universally conserved oligomeric membrane 1.1. Generalities proteins that terminate the respiratory chains of aerobic and facultative aerobic organisms. The structure and function of Cox enzymes have The emerging ease of whole genome sequencing approaches has been studied intensely because of their central role in energy metabo- revealed the existence of multiple terminal oxidases in bacteria, which lism. Given the complexity of these multi-subunit, multi-cofactor en- allow them to utilize efficiently varying oxygen (O2) concentrations in zymes, their assembly also attracted much attention. Indeed, assembly their environments. Most of the terminal oxidases belong to the defects in the human Cox are major causes of mitochondrial disorders, heme-Cu: O2 reductase superfamily (heme-Cu: O2 reductases); they re- and are crucial for neurodegenerative diseases, cancer and aging duce O2 to H2O and couple electron transfer with vectorial proton trans- [4–7]. Among the Cox enzymes, the aa3-type Cox (aa3-Cox) of mito- location across the membrane [1]. Members of this superfamily are chondria and many bacterial species are highly abundant and the present in eukarya, archaea and eubacteria. They are thought to be of best-studied group. However, the heme-Cu: O2 reductases represent a monophyletic origin, possibly related to nitric oxide reductases (NOR) diverse ensemble of enzymes with significantly different subunit com- [2]. NOR catalyze reduction of NO to N2Oduringdenitrification. Al- positions and cofactors [8]. In this review, we focus on the structure, though they do not reduce O2 and do not generate a proton gradient subunit maturation and assembly of the cbb3-type Cox (cbb3-Cox) that [3], their structural organization is similar to heme-Cu: O2 reductases. represent the second most abundant group after the aa3-Cox. Most of The heme-Cu: O2 reductases can be divided into different subgroups the studies on cbb3-Cox biogenesis were performed with the facultative in respect to their electron donors: those that use a c-type cytochrome phototrophic α-proteobacterium Rhodobacter capsulatus. This species is used as a model organism for these studies as it contains only one heme-Cu: O2 reductase, cbb3-Cox. R. capsulatus is still capable of aerobic Abbreviations: Cox, cytochrome c oxidase; Qox, quinol oxidase; Ccm, cytochrome respiration in the absence of it because it also contains an unrelated c maturation; NOR, nitric oxide reductase; BN-PAGE, blue-native polyacrylamide gel terminal oxidase (bd-type quinol oxidase) (Fig. 1) [9,10]. electrophoresis; Cu, Copper ☆ This article is part of a Special Issue entitled: Biogenesis/Assembly of Respiratory Enzyme Complexes. 1.2. Classification of heme-Cu: O2 reductases ⁎ Corresponding author. Tel.: +49 761 203 5250; fax: +49 761 203 5289. ⁎⁎ Corresponding author. Tel.: +1 215 898 4394; fax: +1 215 898 8780. Members of heme-Cu: O reductases are diverse in terms of their E-mail addresses: [email protected] (H.-G. Koch), 2 [email protected] (F. Daldal). subunit composition, heme cofactor content, electron donor, and O2 1 S. Ekici and G. Pawlik are first co-authors for this work. affinity (Table 1) [8,11,12]. All members have a conserved core subunit 0005-2728/$ – see front matter © 2011 Elsevier B.V. All rights reserved. doi:10.1016/j.bbabio.2011.10.011 S. Ekici et al. / Biochimica et Biophysica Acta 1817 (2012) 898–910 899 Fig. 1. The respiratory chain of R. capsulatus and its regulation in response to oxygen availability. The protein complexes and electron carrier of the respiratory chain are shown in yellow. UQ and UQH2 correspond to the oxidized and reduced form of quinones. Soluble cytochrome c2 and the membrane-bound cytochrome cy (indicated as c in the figure) are electron donors for the photosynthetic reaction center and cbb3-Cox. Metabolic processes which also consume redox equivalents are shown in blue. Regulatory proteins are shown in gray. RegB is a sensor kinase that phosphorylates the response regulator RegA under low oxygen concentrations. Phosphorylated RegA (RegA-P) inhibits (shown as the red square) expression of ccoNOQP (cbb3-Cox) and hupSLC ([NiFe] hydrogenase), but stimulates the expression of the bd-type quinol oxidase and of genes required for photosynthesis. In addition, RegA-P stimulates (shown as an arrow) the expression of nifHDK (nitrogenase) and the cbb1 and cbb2 operons (CO2 fixation) both directly and indirectly [154]. Under microaerobic and anaerobic conditions HvrA further represses ccoNOQP expression but stimulates bd-type quinol oxidase expression. Finally, FnrL probably activates ccoNOQP expression in the transition phase between aerobic and anaerobic conditions. R. capsulatus SenC and its R. sphaeroides homologue PrrC were suggested to be involved in oxygen-dependent expression of ccoNOQP and photosynthetic genes. FixLJ-K regulatory system discussed in the text is not shown in the figure. (Subunit I), containing at least 12 transmembrane helices. This subunit conserved Cu and heme cofactor arrangement in these enzymes. Subu- contains a low spin heme (of a-orb-type), a binuclear metal center nit I of type A enzymes contain two proton-transfer pathways referred composed of a high spin heme (of a-, o-, or b-type heme, referred to to as K- and D- channels (Table 1). The four electrons required for O2 re- as a3, o3 or b3)-iron, and a Cu atom (CuB), as well as a tyrosine residue duction at the binuclear heme-CuB center are conveyed sequentially via covalently linked to a histidine ligand of CuB [1,8]. Besides subunit I, a non-covalently attached low spin heme, which itself receives electrons which is the catalytic heart where O2 is reduced to H2O, heme-Cu: O2 from the CuA center in subunit II [15,19]. Type B enzymes are present reductases have at least two other core subunits: Subunit II is the prima- only in bacteria and archaea, but not in eukaryotes, and constitute the ry electron acceptor, and in some cases, it harbors extra cofactors like a least abundant group [20]. The catalytic center of type B enzymes is sim- binuclear Cu center (CuA), or is a c-type cytochrome. Subunit III in many ilar to that of type A, except that they lack the D-channel for proton cases does not contain any cofactor except in cbb3-Cox where it is a transfer [21]. The prototypes of type C are the cbb3-Cox, which are diheme c-type cytochrome (Table 1) [1].MostbacterialCoxarecom- present only in bacteria, and considered to represent the most distant posed of these three core subunits, but mitochondrial Cox are more members of heme-Cu: O2 reductases. They also lack the D-channel for complex with 13 subunits of which only three (subunits I, II, and III) proton transfer [22–24], their subunits II and III are c-type cytochromes are encoded in the mitochondrial genome. An additional fourth subunit (Table 1), and they exhibit higher O2 affinity as compared with other with a single transmembrane helix is also present in some bacterial Cox. types of Cox enzymes. However, this subunit is unlike any of the ten nuclear encoded mito- chondrial subunits [13]. 2. The cbb3-Cox Aclassification, based on common features of the core subunits, and keyresiduesinprotontransferpathways,defines three (A, B and C) 2.1. Distribution of cbb3-Cox in bacteria and its role in pathogenesis types of heme-Cu: O2 reductases (Table 1)(Fig. 2) [1]. Mitochondrial- aa3-Cox (Type A), ba3-Cox of Thermus thermophilus (Type B) and cbb3- The cbb3-Cox enzymes are common to proteobacteria and also Cox of R. capsulatus (Type C) are the most representative members of found in the cytophaga, flexibacter and bacteriodes (CFB) group [12].
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