Abstract
Acetic acid bacteria inhabit sugar-rich niches, especially fruits and flowers, and thus have the ability to utilize sugars or sugar alcohols for their energy sources. The strategy of sugar utilization is rather exceptional: they oxidize such the substrates by “oxidative fermentation” and utilize the accumulated products later. The oxidative fermentation is carried out by the respiratory chain comprising periplasmic primary dehydrogenases of quinoproteins or flavoprotein–cytochrome c complexes and (terminal) ubiquinol oxidases, both of which seem to be acquired by adaptive evolution in such a sugar-rich niche by interacting with other microbes living at the same habitat. In this chapter, the evolution and physiology of such a respiratory chain related to oxidative fermentation are described.
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References
Adachi O, Fujii Y, Ghaly MF, Toyama H, Shinagawa E, Matsushita K (2001) Membrane-bound quinoprotein d-arabitol dehydrogenase of Gluconobacter suboxydans IFO 3257: a versatile enzyme for the oxidative fermentation of various ketoses. Biosci Biotechnol Biochem 65:2755–2762
Asai T (1968) Acetic acid bacteria. Classification and biochemical activities. Tokyo University Press, Tokyo
Azuma Y, Hosoyama A, Matsutani M, Furuya N, Horikawa H, Harada T, Hirakawa H, Kuhara S, Matsushita K, Fujita N, Shirai M (2009) Whole-genome analyses reveal genetic instability of Acetobacter pasteurianus. Nucleic Acids Res 37:5768–5783
Bertalan M et al (2009) Complete genome sequence of the sugarcane nitrogen-fixing endophyte Gluconacetobacter diazotrophicus Pal5. BMC Genomics 10:450
Castresana J, Lübben M, Saraste M, Higgins DG (1994) Evolution of cytochrome oxidase, an enzyme older than atmospheric oxygen. EMBO J 13:2516–2525
Cleton-Jansen AM, Goosen N, Vink K, van de Putte P (1989) Cloning, characterization and DNA sequencing of the gene encoding the M r 50,000-quinoprotein glucosedehydrogenase from Acinetobacter calcoaceticus. Mol Gen Genet 217:430–436
Gao L, Du G, Zhou J, Chen J, Liu J (2013) Characterization of a group of pyrroloquinoline quinone-dependent dehydrogenases that are involved in the conversion of l-sorbose to 2-keto-l-gluconic acid in Ketogulonicigenium vulgare WSH-001. Biotechnol Prog 29:1398–1404
Görisch H, Rupp M (1989) Quinoprotein ethanol dehydrogenase from Pseudomonas. Antonie Van Leeuwenhoek 56:35–45
Greenberg DE, Porcella SF, Zelazny AM, Virtaneva K, Sturdevant DE, Kupko JJ 3rd, Barbian KD, Babar A, Dorward DW, Holland SM (2007) Genome sequence analysis of the emerging human pathogenic acetic acid bacterium Granulibacter bethesdensis. J Bacteriol 189:8727–8736
Groen BW, van Kleef MA, Duine JA (1986) Quinohaemoprotein alcohol dehydrogenase apoenzyme from Pseudomonas testosteroni. Biochem J 234:611–615
Hagan CL, Kim S, Kahne D (2010) Reconstitution of outer membrane protein assembly from purified components. Science 328:890–892
Higashiura N, Hadano H, Hirakawa H, Matsutani M, Takebe S, Matsushita K, Azuma Y (2014) Draft genomic DNA sequence of the facultatively methylotrophic bacterium Acidomonas methanolica type strain MB58. FEMS Microbiol Lett 351:9–13
Hölscher T, Weinert-Sepalage D, Görisch H (2007) Identification of membrane-bound quinoprotein inositol dehydrogenase in Gluconobacter oxydans ATCC 621H. Microbiology 153:499–506
Inose K, Fujikawa M, Yamazaki T, Kojima K, Sode K (2003) Cloning and expression of the gene encoding catalytic subunit of thermostable glucose dehydrogenase from Burkholderia cepacia in Escherichia coli. Biochim Biophys Acta 1645:133–138
Kataoka N, Matsutani M, Yakushi T, Matsushita K (2015) Efficient production of 2,5-diketo-d-gluconate via heterologous expression of 2-keto-gluconate dehydrogenase in Gluconobacter japonicus. Appl Environ Microbiol 81:3552–3560
Kawai S, Goda-Tsutsumi M, Yakushi T, Kano K, Matsushita K (2013) Heterologous overexpression and characterization of a flavoprotein-cytochrome c complex fructose dehydrogenase of Gluconobacter japonicus NBRC3260. Appl Environ Microbiol 79:1654–1660
Kita K, Konishi K, Anraku Y (1984) Terminal oxidases of Escherichia coli aerobic respiratory chain. I. Purification and properties of cytochrome b 562-o complex from cells in the early exponential phase of aerobic growth. J Biol Chem 259:3368–3374
Matsushita K, Adachi O (1993) Bacterial quinoproteins glucose dehydrogenase and alcohol dehydrogenase. In: Davidson V (ed) Principles and applications of quinoproteins. Dekker, New York, pp 47–63
Matsushita K, Shinagawa E, Ameyama M (1982) d-Gluconate dehydrogenase from bacteria, 2-keto-d-gluconate-yielding, membrane-bound. Methods Enzymol 89:187–193
Matsushita K, Patel L, Kaback HR (1984) Cytochrome o type oxidase from Escherichia coli. Characterization of the enzyme and mechanism of electrochemical proton gradient generation. Biochemistry 23:4703–4714
Matsushita K, Ebisuya H, Adachi O (1992a) Homology in the structure and the prosthetic groups between two different terminal ubiquinol oxidases, cytochrome a 1 and cytochrome o, of Acetobacter aceti. J Biol Chem 267:24748–24753
Matsushita K, Takahashi K, Takahashi M, Ameyama M, Adachi O (1992b) Methanol and ethanol oxidase respiratory chains of the methylotrophic acetic acid bacterium, Acetobacter methanolicus. J Biochem (Tokyo) 111:739–747
Matsushita K, Toyama H, Adachi O (1994) Respiratory chains and bioenergetics of acetic acid bacteria. Adv Microb Physiol 36:247–301
Matsushita K, Toyama H, Yamada M, Adachi O (2002) Quinoproteins: structure, function, and biotechnological applications. Appl Microbiol Biotechnol 58:13–22
Matsushita K, Fujii Y, Ano Y, Toyama H, Shinjoh M, Tomiyama N, Miyazaki T, Sugisawa T, Hoshino T, Adachi O (2003) 5-Keto-d-gluconate production is catalyzed by a quinoprotein glycerol dehydrogenase, major polyol dehydrogenase, in Gluconobacter species. Appl Environ Microbiol 69:1959–1966
Matsushita K, Inoue T, Theeragool G, Trcek J, Toyama H, Adachi O (2005) Acetic acid production in acetic acid bacteria leading to their ‘death’ and survival. In: Yamada M (ed) Survival and death in bacteria. Research Signpost, Kerala, pp 169–181
Matsushita K, Kobayashi Y, Mizuguchi M, Toyama H, Adachi O, Sakamoto K, Miyoshi H (2008) A tightly bound quinone functions in ubiquinone reaction sites of quinoprotein alcohol dehydrogenase of acetic acid bacteria, Gluconobacter suboxydans. Biosci Biotechnol Biochem 72:2723–2731
Matsutani M, Hirakawa H, Yakushi T, Matsushita K (2011) Genome-wide phylogenetic analysis of Gluconobacter, Acetobacter, and Gluconacetobacter. FEMS Microbiol Lett 315:122–128
Matsutani M, Fukushima K, Kayama C, Arimitsu M, Hirakawa H, Toyama H, Adachi O, Yakushi T, Matsushita K (2014a) Replacement of a terminal cytochrome c oxidase by ubiquinol oxidase during the evolution of acetic acid bacteria. Biochim Biophys Acta Bioenerg 1837:1810–1820
Matsutani M, Suzuki H, Yakushi T, Matsushita K (2014b) Draft genome sequence of Gluconobacter thailandicus NBRC 3257. Stand Genomic Sci 9:614–623
Miura H, Mogi T, Ano Y, Migita CT, Matsutani M, Yakushi T, Kita K, Matsushita K (2013) Cyanide-insensitive quinol oxidase (CIO) from Gluconobacter oxydans is a unique terminal oxidase subfamily of cytochrome bd. J Biochem (Tokyo) 153:535–545
Miyazaki T, Tomiyama N, Shinjoh M, Hoshino T (2002) Molecular cloning and functional expression of d-sorbitol dehydrogenase from Gluconobacter suboxydans IFO3255, which requires pyrroloquinoline quinone and hydrophobic protein SldB for activity development in E. coli. Biosci Biotechnol Biochem 66:262–270
Miyazaki T, Sugisawa T, Hoshino T (2006) Pyrroloquinoline quinone-dependent dehydrogenases from Ketogulonicigenium vulgare catalyze the direct conversion of l-sorbosone to l-ascorbic acid. Appl Environ Microbiol 72:1487–1495
Ogino H, Azuma Y, Hosoyama A, Nakazawa H, Matsutani M, Hasegawa A, Otsuyama K, Matsushita K, Fujita N, Shirai M (2011) Complete genome sequence of NBRC 3288, a unique cellulose-nonproducing strain of Gluconacetobacter xylinus isolated from vinegar. J Bacteriol 193:6997–6998
Oubrie A (2003) Structure and mechanism of soluble glucose dehydrogenase and other PQQ-dependent enzymes. Biochim Biophys Acta 1647:143–151
Peters B, Mientus M, Kostner D, Junker A, Liebl W, Ehrenreich A (2013) Characterization of membrane-bound dehydrogenases from Gluconobacter oxydans 621H via whole-cell activity assays using multideletion strains. Appl Microbiol Biotechnol 97:6397–6412
Prust C, Hoffmeister M, Liesegang H, Wiezer A, Fricke WF, Ehrenreich A, Gottschalk G, Deppenmeier U (2005) Complete genome sequence of the acetic acid bacterium Gluconobacter oxydans. Nat Biotechnol 23:195–200
Pujol CJ, Kado CI (2000) Genetic and biochemical characterization of the pathway in Pantoea citrea leading to pink disease of pineapple. J Bacteriol 182:2230–2237
Richhardt J, Bringer S, Bott M (2012) Mutational analysis of the pentose phosphate and Entner–Doudoroff pathways in Gluconobacter oxydans reveals improved growth of a Δedd Δeda mutant on mannitol. Appl Environ Microbiol 78:6975–6986
Saichana I, Moonmangmee D, Adachi O, Matsushita K, Toyama H (2009) Screening of thermotolerant Gluconobacter strains for production of 5-keto-d-gluconic acid and disruption of flavin adenine dinucleotide-containing d-gluconate dehydrogenase. Appl Environ Microbiol 75:4240–4247
Saiki K, Mogi T, Anraku Y (1992) Heme O biosynthesis in Escherichia coli: the cyoE gene in the cytochrome bo operon encodes a protoheme IX farnesyltransferase. Biochem Biophys Res Commun 189:1491–1497
Sakurai K, Yamazaki S, Ishii M, Igarashi Y, Arai H (2013) Role of the glyoxylate pathway in acetic acid production by Acetobacter aceti. J Biosci Bioeng 115:32–36
Shinagawa E, Matsushita K, Adachi O, Ameyama M (1984) d-Gluconate dehydrogenase, 2-keto-d-gluconate yielding, from Gluconobacter dioxyacetonicus: purification and characterization. Agric Biol Chem 48:1517–1522
Swings J, Gillis M, Kersters K, De Vos P, Gossle F, De Ley J (1980) Frateuria, a new genus for “Acetobacter aurantius”. Int J Syst Bacteriol 30:547–556
Toyama H, Mathews FS, Adachi O, Matsushita K (2004) Quinohemoprotein alcohol dehydrogenases: structure, function, and physiology. Arch Biochem Biophys 428:10–21
Toyama H, Soemphol W, Moonmangmee D, Adachi O, Matsushita K (2005) Molecular properties of membrane-bound FAD-containing d-sorbitol dehydrogenase from thermotolerant Gluconobacter frateurii isolated from Thailand. Biosci Biotechnol Biochem 69:1120–1129
Toyama H, Furuya N, Saichana I, Ano Y, Adachi O, Matsushita K (2007) Membrane-bound, 2-keto-d-gluconate-yielding d-gluconate dehydrogenase from “Gluconobacter dioxyacetonicus” IFO 3271: molecular properties and gene disruption. Appl Environ Microbiol 73:6551–6556
Trček J, Matsushita K (2013) A unique enzyme of acetic acid bacteria, PQQ-dependent alcohol dehydrogenase, is also present in Frateuria aurantia. Appl Microbiol Biotechnol 97:7369–7376
Van Spanning RJ, Wansell CW, De Boer T, Hazelaar MJ, Anazawa H, Harms N, Oltmann LF, Stouthamer AH (1991) Isolation and characterization of the moxJ, moxG, moxI, and moxR genes of Paracoccus denitrificans: inactivation of moxJ, moxG, and moxR and the resultant effect on methylotrophic growth. J Bacteriol 173:6948–6961
Vangnai AS, Toyama H, De-Eknamkul W, Yoshihara N, Adachi O, Matsushita K (2004) Quinate oxidation in Gluconobacter oxydans IFO3244: purification and characterization of quinoprotein quinate dehydrogenase. FEMS Microbiol Lett 241:157–162
Yamada M, Sumi K, Matsushita K, Adachi O, Yamada Y (1993) Topological analysis of quinoprotein glucose dehydrogenase in Escherichia coli and its ubiquinone-binding site. J Biol Chem 268:12812–12817
Yang T (1986) Biochemical and biophysical properties of cytochrome o of Azotobacter vinelandii. Biochim Biophys Acta 848:342–351
Yum DY, Lee YP, Pan JG (1997) Cloning and expression of a gene cluster encoding three subunits of membrane-bound gluconate dehydrogenase from Erwinia cypripedii ATCC 29267 in Escherichia coli. J Bacteriol 179:6566–6572
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Matsushita, K., Matsutani, M. (2016). Distribution, Evolution, and Physiology of Oxidative Fermentation. In: Matsushita, K., Toyama, H., Tonouchi, N., Okamoto-Kainuma, A. (eds) Acetic Acid Bacteria. Springer, Tokyo. https://doi.org/10.1007/978-4-431-55933-7_7
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DOI: https://doi.org/10.1007/978-4-431-55933-7_7
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