A novel scenario for the evolution of haem–copper oxygen reductases

Abstract

The increasing sequence information on oxygen reductases of the haem-copper superfamily, together with the available three-dimensional structures, allows a clear identification of their common, functionally important features. Taking into consideration both the overall amino acid sequences of the core subunits and key residues involved in proton transfer, a novel hypothesis for the molecular evolution of these enzymes is proposed. Three main families of oxygen reductases are identified on the basis of common features of the core subunits, constituting three lines of evolution: (i) type A (mitochondrial-like oxidases), (ii) type B (ba3-like oxidases) and (iii) type C (cbb3-type oxidases). The first group can be further divided into two subfamilies, according to the helix VI residues at the hydrophobic end of one of the proton pathways (the so-called D-channel): (i) type A1, comprising the enzymes with a glutamate residue in the motif -XGHPEV-, and (ii) type A2, enzymes having instead a tyrosine and a serine in the alternative motif -YSHPXV-. This second subfamily of oxidases is shown to be ancestor to the one containing the glutamate residue, which in the Bacteria domain is only present in oxidases from Gram-positive or purple bacteria. It is further proposed that the Archaea domain acquired terminal oxidases by gene transfer from the Gram-positive bacteria, implying that these enzymes were not present in the last common ancestor before the divergence between Archaea and Bacteria. In fact, most oxidases from archaea have a higher amino acid sequence identity and similarity with those from bacteria, mainly from the Gram-positive group, than with oxidases from other archaea. Finally, a possible relation between the dihaemic subunit (FixP) of the cbb3 oxidases and subunit II of caa3 oxidases is discussed. As the families of haem-copper oxidases can also be identified by their subunit II, a parallel evolution of subunits I and II is suggested.

Crystal structures of nitric oxide reductases provide key insights into functional conversion of respiratory enzymes

“…In Aand B-type COXs, on the other hand, positively charged groups from two conserved arginine residues locate at the equivalent position to the Ca ion (18)(19)(20)(21). It is therefore likely that NORs and C-type COX are closely related to one another and are evolutionary distinct from A-and B-type COXs, which is consistent with the view from the phylogenetic analysis (7,22).…”

“…2H 2 O), shows sequence similarities to NOR (4,5). Phylogenetic analysis suggested that NOR and COX are classified as members of the heme-copper oxidase superfamily and share the same ancestor protein (5)(6)(7). NORs and some COXs have crossreactivity with respective substrate (8)(9)(10), further supporting the view that NOR is evolutionary related to COX.…”

Aerobic growth at nanomolar oxygen concentrations

“…Independent of these geological arguments, the history of oxidase enzymes places other constraints on the origins of aerobiosis (30,43,44). Although there is active debate on the phylogenetic history of oxidase enzymes, recent models (30,43,44) support an ancient origin, even before the evolution of oxygen-producing cyanobacteria (45). Without a cyanobacterial source, oxygen could have come from abiotic sources, such as the rainout and disproportionation (by catalase enzymes) of atmospherically produced H 2 O 2 at the Earth's surface.…”

Regulation of the aerobic respiratory chain in the facultatively aerobic and hyperthermophilic archaeon Pyrobaculum oguniense

“…The residues for the K channel of proton pumping are conserved in both oxidases (PoxC: Y257, S268, S328, K331; and PoxI: Y223, S234, S295, Y299). On the other hand, the residues necessary for the D channel of haem-copper oxidases are conserved in PoxC (N89, N107, D100, T165, F251, G252 and E255), but are not conserved in PoxI as for other known SoxB-type haem-copper oxidases like those of Sulfolobus acidocaldarius, Acidianus ambivalens, Thermus thermophilus and Geobacillus stearothermophilus (Riistama et al, 1996;Purschke et al, 1997;Keightley et al, 1995;Nikaido et al, 1998;Pereira et al, 2001 poxJ encodes a homologue of scoI of Saccharomyces cerevisiae that is widely conserved in eukarya, proteobacteria and Aquifex aeolicus (Chinenov, 2000). Alignment of ScoI-related proteins showed that PoxJ contained Cu(I)-binding residues (C84, C88 and H169) (Nittis et al, 2001).…”