Abstract
Acetone and other ketones are activated for subsequent degradation through carboxylation by many nitrate-reducing, phototrophic, and obligately aerobic bacteria. Acetone carboxylation leads to acetoacetate, which is subsequently activated to a thioester and degraded via thiolysis. Two different types of acetone carboxylases have been described, which require either 2 or 4 ATP equivalents as an energy supply for the carboxylation reaction. Both enzymes appear to combine acetone enolphosphate with carbonic phosphate to form acetoacetate. A similar but more complex enzyme is known to carboxylate the aromatic ketone acetophenone, a metabolic intermediate in anaerobic ethylbenzene metabolism in denitrifying bacteria, with simultaneous hydrolysis of 2 ATP to 2 ADP. Obligately anaerobic sulfate-reducing bacteria activate acetone to a four-carbon compound as well, but via a different process than bicarbonate- or CO2-dependent carboxylation. The present evidence indicates that either carbon monoxide or a formyl residue is used as a cosubstrate, and that the overall ATP expenditure of this pathway is substantially lower than in the known acetone carboxylase reactions.
Journal Section:
Review Article
Keywords:
Carboxylation,
Hydrocarbons,
Ketones,
Energetics,
ATP,
Carbon monoxide,
Thiamine diphosphate,
Formate
References
1.
Abu Laban N, Selesi D, Rattei T, Tischler P, Meckenstock RU: Identification of enzymes involved in anaerobic benzene degradation by a strictly anaerobic iron-reducing enrichment culture. Environ Microbiol 2010;12:2783-2796.
[PubMed]
2.
Allen JR, Ensign SA: Carboxylation of epoxides to beta-keto acids in cell extracts of Xanthobacter strain Py2. J Bacteriol 1996;178:1469-1472.
[PubMed]
3.
Birks SJ, Kelly DJ: Assay and properties of acetone carboxylase, a novel enzyme involved in acetone-dependent growth and CO2 fixation in Rhodobacter capsulatus and other photosynthetic and denitrifying bacteria. Microbiology 1997;143:755-766.
4.
Bonnet-Smits E, Robertson L, Van Dijken J, Senior E, Kuenen J: Carbon dioxide fixation as the initial step in the metabolism of acetone by Thiosphaera pantotropha. J Gen Microbiol 1988;134:2281-2289.
5.
Boyd JM, Ellsworth H, Ensign SA: Bacterial acetone carboxylase is a manganese-dependent metalloenzyme. J Biol Chem 2004;279:46644-46651.
[PubMed]
6.
Boyd JM, Ensign SA: ATP-dependent enolization of acetone by acetone carboxylase from Rhodobacter capsulatus. Biochemistry 2005;44:8543-8553.
[PubMed]
7.
Brahmachary P, Wang G, Benoit SL, Weinberg MV, Maier RJ, Hoover TR: The human gastric pathogen Helicobacter pylori has a potential acetone carboxylase that enhances its ability to colonize mice. BMC Microbiol 2008;8:14.
[PubMed]
8.
Casteels M, Sniekers M, Fraccascia P, Mannaerts G, Van Veldhoven PP: The role of 2-hydroxyacyl-CoA lyase, a thiamin pyrophosphate-dependent enzyme, in the peroxisomal metabolism of 3-methyl-branched fatty acids and 2-hydroxy straight-chain fatty acids. Biochem Soc Trans 2007;35:876-880.
[PubMed]
9.
Clark DD, Ensign SA: Evidence for an inducible nucleotide-dependent acetone carboxylase in Rhodococcus rhodochrous B276. J Bacteriol 1999;181:2752-2758.
[PubMed]
10.
Dullius CH, Chen C-Y, Schink B: Nitrate-dependent degradation of acetone by Alicycliphilus and Paracoccus strains and comparison of acetone carboxylase enzymes. Appl Environ Microbiol 2011;77:6821-6825.
[PubMed]
11.
Ensign SA, Allen JR: Aliphatic epoxide carboxylation. Annu Rev Biochem 2003;72:55-76.
[PubMed]
12.
Ensign SA, Small FJ, Allen JR, Sluis MK: New roles for CO2 in the microbial metabolism of aliphatic epoxides and ketones. Arch Microbiol 1998;169:179-187.
[PubMed]
13.
Fuchs G, Boll M, Heider J: Microbial degradation of aromatic compounds - from one strategy to four. Nat Rev Microbiol 2011;9:803-816.
[PubMed]
14.
Gallert C, Knoll G, Winter J: Anaerobic carboxylation of phenol to benzoate: use of deuterated phenols revealed carboxylation exclusively in the C4-position. Appl Microbiol Biotechnol 1991;36:124-129.
15.
Gallert C, Winter J: Comparison of 4-hydroxynzoate decarboxylase and phenol carboxylase activities in cell-free extracts of a defined, 4-hydroxybenzoate and phenol-degrading anaerobic consortium. Appl Microbiol Biotechnol 1992;37:119-124.
16.
Gutiérrez Acosta OB, Hardt N, Hacker SM, Strittmatter T, Schink B, Marx A: Thiamine pyrophosphate stimulates acetone activation by Desulfococcus biacutus as monitored by a fluorogenic ATP analogue. ACS Chem Biol 2014b;9:1263-1266.
[PubMed]
17.
Gutiérrez Acosta OB, Hardt N, Schink B: Carbonylation as a key reaction in anaerobic acetone activation by Desulfococcus biacutus. Appl Environ Microbiol 2013;79:6228-6235.
[PubMed]
18.
Gutiérrez Acosta OB, Schleheck D, Schink B: Acetone utilization by sulfate-reducing bacteria: draft genome sequence of Desulfococcus biacutus and a proteomic survey of acetone-inducible proteins. BMC Genomics 2014a;15:584.
[PubMed]
19.
Haritash A, Kaushik C: Biodegradation aspects of polycyclic aromatic hydrocarbons (PAHs): a review. J Hazard Mater 2009;169:1-15.
[PubMed]
20.
Heider J: Adding handles to unhandy substrates: anaerobic hydrocarbon activation mechanisms. Curr Opin Chem Biol 2007;11:188-194.
[PubMed]
21.
Janssen PH, Schink B: Catabolic and anabolic enzyme activities and energetics of acetone metabolism of the sulfate-reducing bacterium Desulfococcus biacutus. J Bacteriol 1995a;177:277-282.
[PubMed]
22.
Janssen PH, Schink B: Metabolic pathways and energetics of the acetone-oxidizing, sulfate-reducing bacterium, Desulfobacterium cetonicum. Arch Microbiol 1995b;163:188-194.
[PubMed]
23.
Jobst B, Schühle K, Linne U, Heider J: ATP-dependent carboxylation of acetophenone by a novel type of carboxylase. J Bacteriol 2010;192:1387-1394.
[PubMed]
24.
Kai Y, Matsumura H, Izui K: Phosphoenolpyruvate carboxylase: three-dimensional structure and molecular mechanisms. Arch Biochem Biophys 2003;414:170-179.
[PubMed]
25.
Kniemeyer O, Heider J: Ethylbenzene dehydrogenase, a novel hydrocarbon-oxidizing molybdenum/iron-sulfur/heme enzyme. J Biol Chem 2001a;276:21381-21386.
[PubMed]
26.
Kniemeyer O, Heider J: (S)-1-Phenylethanol dehydrogenase of Azoarcus sp. strain EbN1, an enzyme of anaerobic ethylbenzene catabolism. Arch Microbiol 2001b;176:129-135.
[PubMed]
27.
Kotani T, Yurimoto H, Kato N, Sakai Y: Novel acetone metabolism in a propane-utilizing bacterium, Gordonia sp. strain TY-5. J Bacteriol 2007;189:886-893.
[PubMed]
28.
Kühner S, Wöhlbrand L, Fritz I, Wruck W, Hultschig C, Hufnagel P, Kube M, Reinhardt R, Rabus R: Substrate-dependent regulation of anaerobic degradation pathways for toluene and ethylbenzene in a denitrifying bacterium, strain EbN1. J Bacteriol 2005;187:1493-1503.
[PubMed]
29.
Lack A, Fuchs G: Carboxylation of phenylphosphate by phenol carboxylase, an enzyme system of anaerobic phenol metabolism. J Bacteriol 1992;174:3629-3636.
[PubMed]
30.
Lack A, Fuchs G: Evidence that phenol phosphorylation to phenylphosphate is the first step in anaerobic phenol metabolism in a denitrifying Pseudomonas sp. Arch Microbiol 1994;161:132-139.
[PubMed]
31.
Lukins H, Foster J: Methyl ketone metabolism in hydrocarbon-utilizing mycobacteria. J Bacteriol 1963;85:1074-1087.
[PubMed]
32.
McMahon RJ: Biotin in metabolism and molecular biology. Annu Rev Nutr 2002;22:221-239.
[PubMed]
33.
Meckenstock RU, Mouttaki H: Anaerobic degradation of non-substituted aromatic hydrocarbons. Curr Opin Biotechnol 2011;22:406-414.
[PubMed]
34.
Mouttaki H, Johannes J, Meckenstock RU: Identification of naphthalene carboxylase as a prototype for the anaerobic activation of non-substituted aromatic hydrocarbons. Environ Microbiol 2012;14:2770-2774.
[PubMed]
35.
Nocek B, Boyd J, Ensign SA, Peters JW: Crystallization and preliminary X-ray analysis of an acetone carboxylase from Xanthobacter autotrophicus strain Py2. Acta Crystallogr D Biol Crystallogr 2004;60:385-387.
[PubMed]
36.
Ogawa J, Kim JM, Nirdnoy W, Amano Y, Yamada H, Shimizu S: Purification and characterization of an ATP-dependent amidohydrolase, N-methylhydantoin amidohydrolase, from Pseudomonas putida 77. Eur J Biochem 1995;229:284-290.
[PubMed]
37.
Oosterkamp MJ, Boeren S, Atashgahi S, Plugge CM, Schaap PJ, Stams AJ: Proteomic analysis of nitrate-dependent acetone degradation by Alicycliphilus denitrificans strain BC. FEMS Microbiol Lett 2015:fnv080.
[PubMed]
38.
Platen H, Schink B: Methanogenic degradation of acetone by an enrichment culture. Arch Microbiol 1987;149:136-141.
[PubMed]
39.
Platen H, Schink B: Anaerobic degradation of acetone and higher ketones via carboxylation by newly isolated denitrifying bacteria. J Gen Microbiol 1989;135:883-891.
[PubMed]
40.
Platen H, Temmes A, Schink B: Anaerobic degradation of acetone by Desulfococcus biacutus spec. nov. Arch Microbiol 1990;154:355-361.
[PubMed]
41.
Rabus R, Kube M, Beck A, Widdel F, Reinhardt R: Genes involved in the anaerobic degradation of ethylbenzene in a denitrifying bacterium, strain EbN1. Arch Microbiol 2002;178:506-516.
[PubMed]
42.
Rabus R, Widdel F: Anaerobic degradation of ethylbenzene and other aromatic hydrocarbons by new denitrifying bacteria. Arch Microbiol 1995;163:96-103.
[PubMed]
43.
Rosier C, Leys N, Henoumont C, Mergeay M, Wattiez R: Purification and characterization of the acetone carboxylase of Cupriavidus metallidurans strain CH34. Appl Environ Microbiol 2012;78:4516-4518.
[PubMed]
44.
Schnell S, Schink B: Anaerobic aniline degradation via reductive deamination of 4-aminobenzoyl-CoA in Desulfobacterium anilini. Arch Microbiol 1991;155:183-190.
45.
Schühle K, Fuchs G: Phenylphosphate carboxylase: a new CC lyase involved in anaerobic phenol metabolism in Thauera aromatica. J Bacteriol 2004;186:4556-4567.
[PubMed]
46.
Schühle K, Heider J: Acetone and butanone metabolism of the denitrifying bacterium ‘Aromatoleum aromaticum' demonstrates novel biochemical properties of an ATP-dependent aliphatic ketone carboxylase. J Bacteriol 2012;194:131-141.
[PubMed]
47.
Sluis MK, Ensign SA: Purification and characterization of acetone carboxylase from Xanthobacter strain Py2. Proc Natl Acad Sci USA 1997;94:8456-8461.
[PubMed]
48.
Sluis MK, Larsen RA, Krum JG, Anderson R, Metcalf WW, Ensign SA: Biochemical, molecular, and genetic analyses of the acetone carboxylases from Xanthobacter autotrophicus strain Py2 and Rhodobacter capsulatus strain B10. J Bacteriol 2002;184:2969-2977.
[PubMed]
49.
Sluis MK, Small FJ, Allen JR, Ensign SA: Involvement of an ATP-dependent carboxylase in a CO2-dependent pathway of acetone metabolism by Xanthobacter strain Py2. J Bacteriol 1996;178:4020-4026.
[PubMed]
50.
Taylor BL, Zhulin IB: PAS domains: internal sensors of oxygen, redox potential, and light. Microbiol Mol Biol Rev 1999;63:479-506.
[PubMed]
51.
Taylor DG, Trudgill PW, Cripps RE, Harris PR: The microbial metabolism of acetone. J Gen Microbiol 1980;118:159-170.
52.
Thauer RK, Jungermann K, Decker K: Energy conservation in chemotrophic anaerobic bacteria. Bacteriol Rev 1977;41:100.
[PubMed]
53.
Tschech A, Fuchs G: Anaerobic degradation of phenol by pure cultures of newly isolated denitrifying pseudomonads. Arch Microbiol 1987;148:213-217.
[PubMed]
54.
Tschech A, Fuchs G: Anaerobic degradation of phenol via carboxylation to 4-hydroxybenzoate: in vitro study of isotope exchange between 14CO2 and 4-hydroxybenzoate. Arch Microbiol 1989;152:594-599.
55.
Wentzel A, Ellingsen TE, Kotlar H-K, Zotchev SB, Throne-Holst M: Bacterial metabolism of long-chain n-alkanes. Appl Microbiol Biotechnol 2007;76:1209-1221.
[PubMed]
56.
Widdel F, Knittel K, Galushko A: Anaerobic hydrocarbon-degrading microorganisms: an overview; in Timmis K (ed): Handbook of Hydrocarbon and Lipid Microbiology. Berlin/Heidelberg, Springer, 2010, pp 1997-2021.
57.
Wöhlbrand L, Kallerhoff B, Lange D, Hufnagel P, Thiermann J, Reinhardt R, Rabus R: Functional proteomic view of metabolic regulation in ‘Aromatoleum aromaticum' strain EbN1. Proteomics 2007;7:2222-2239.
[PubMed]
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