title: Replacement of a terminal cytochrome c oxidase by ubiquinol oxidase during the evolution of acetic acid bacteria.
abstract: The bacterial aerobic respiratory chain has a terminal oxidase of the heme-copper oxidase superfamily, comprised of cytochrome c oxidase (COX) and ubiquinol oxidase (UOX); UOX evolved from COX. Acetobacter pasteurianus, an α-Proteobacterial acetic acid bacterium (AAB), produces UOX but not COX, although it has a partial COX gene cluster, ctaBD and ctaA, in addition to the UOX operon cyaBACD. We expressed ctaB and ctaA genes of A. pasteurianus in Escherichia coli and demonstrated their function as heme O and heme A synthases. We also found that the absence of ctaD function is likely due to accumulated mutations. These COX genes are closely related to other α-Proteobacterial COX proteins. However, the UOX operons of AAB are closely related to those of the β/γ-Proteobacteria (γ-type UOX), distinct from the α/β-Proteobacterial proteins (α-type UOX), but different from the other γ-type UOX proteins by the absence of the cyoE heme O synthase. Thus, we suggest that A. pasteurianus has a functional γ-type UOX but has lost the COX genes, with the exception of ctaB and ctaA, which supply the heme O and A moieties for UOX. Our results suggest that, in AAB, COX was replaced by β/γ-Proteobacterial UOX via horizontal gene transfer, while the COX genes, except for the heme O/A synthase genes, were lost.
authors.affiliation: Department of Biological Chemistry, Faculty of Agriculture, Yamaguchi University, Yamaguchi, Yamaguchi 753-8515, Japan.
authors.forename: Minenosuke
authors.initials: M
authors.lastname: Matsutani
authors.affiliation: Department of Biological Chemistry, Faculty of Agriculture, Yamaguchi University, Yamaguchi, Yamaguchi 753-8515, Japan.
authors.forename: Kota
authors.initials: K
authors.lastname: Fukushima
authors.affiliation: Department of Biological Chemistry, Faculty of Agriculture, Yamaguchi University, Yamaguchi, Yamaguchi 753-8515, Japan.
authors.forename: Chiho
authors.initials: C
authors.lastname: Kayama
authors.affiliation: Department of Biological Chemistry, Faculty of Agriculture, Yamaguchi University, Yamaguchi, Yamaguchi 753-8515, Japan.
authors.forename: Misato
authors.initials: M
authors.lastname: Arimitsu
authors.affiliation: Laboratory of Applied Plant Genomics, Department of Plant Genome Research, Kazusa DNA Research Institute, 2-6-7 Kazusakamatari, Kisarazu, Chiba 292-0818, Japan.
authors.forename: Hideki
authors.initials: H
authors.lastname: Hirakawa
authors.affiliation: Department of Biological Chemistry, Faculty of Agriculture, Yamaguchi University, Yamaguchi, Yamaguchi 753-8515, Japan.
authors.forename: Hirohide
authors.initials: H
authors.lastname: Toyama
authors.affiliation: Department of Biological Chemistry, Faculty of Agriculture, Yamaguchi University, Yamaguchi, Yamaguchi 753-8515, Japan.
authors.forename: Osao
authors.initials: O
authors.lastname: Adachi
authors.affiliation: Department of Biological Chemistry, Faculty of Agriculture, Yamaguchi University, Yamaguchi, Yamaguchi 753-8515, Japan.
authors.forename: Toshiharu
authors.initials: T
authors.lastname: Yakushi
authors.affiliation: Department of Biological Chemistry, Faculty of Agriculture, Yamaguchi University, Yamaguchi, Yamaguchi 753-8515, Japan. Electronic address: kazunobu@yamaguchi-u.ac.jp.
authors.forename: Kazunobu
authors.initials: K
authors.lastname: Matsushita
mesh_terms: D000091:Acetobacter / Q000201:enzymology / Q000235:genetics / Q000378:metabolism*; D005075:Biological Evolution; D003576:Electron Transport Complex IV / Q000378:metabolism*; D004926:Escherichia coli / Q000235:genetics; D005798:Genes, Bacterial; D010088:Oxidoreductases / Q000378:metabolism*; D010802:Phylogeny
chemical_list: D010088:Oxidoreductases; C432586:ubiquinol oxidase; D003576:Electron Transport Complex IV
keywords: Acetic acid bacteria; Cytochrome c oxidase; Heme synthase; Heme-copper oxidase; Horizontal gene transfer; Ubiquinol oxidase