Two reactions are simultaneously catalyzed by a single enzyme: The arginine-dependent simultaneous formation of two products, ethylene and succinate, from 2-oxoglutarate by an enzyme from Pseudomonas syringae

Fukuda, Hideo; Ogawa, Takahira; Tazaki, Masato; Nagahama, Kazuhiro; Fujiil, Takao; Tanase, Sumio; Morino, Yoshimasa

doi:10.1016/0006-291x(92)91081-z

Cited by 88 publications

(89 citation statements)

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“…1A) (5-7). Ethylene is also produced in some microorganisms by oxidation of 2-oxo-4-methylthiobutyric acid in a reaction not directly enzyme catalyzed (8,9).In work aimed at producing industrial ethylene by biocatalysis, Pseudomonas strains, including plant pathogens, were shown to produce large amounts of ethylene (10)(11)(12)(13)(14). Bacteria engineered to produce ethylene using the Pseudomonas syringae pv.…”

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“…In work aimed at producing industrial ethylene by biocatalysis, Pseudomonas strains, including plant pathogens, were shown to produce large amounts of ethylene (10)(11)(12)(13)(14). Bacteria engineered to produce ethylene using the Pseudomonas syringae pv.…”

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confidence: 99%

“…PsEFE-catalyzed ethylene production is 2OG-dependent and is stimulated by the addition of L-arginine (L-Arg), which is also converted by PsEFE into pyrroline-5-carboxylate (P5C; Fig. 1B) (13,20). In contrast to the consensus 2OG oxygenase mechanism, which involves sequential binding of 2OG, substrate, and then oxygen, an unprecedented "dual circuit" mechanism is proposed for PsEFE (13).…”

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confidence: 99%

“…1B) (13,20). In contrast to the consensus 2OG oxygenase mechanism, which involves sequential binding of 2OG, substrate, and then oxygen, an unprecedented "dual circuit" mechanism is proposed for PsEFE (13).…”

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Structural and stereoelectronic insights into oxygenase-catalyzed formation of ethylene from 2-oxoglutarate

Zhang

Smart

Choi

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

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Ethylene is important in industry and biological signaling. In plants, ethylene is produced by oxidation of 1-aminocyclopropane-1-carboxylic acid, as catalyzed by 1-aminocyclopropane-1-carboxylic acid oxidase. Bacteria catalyze ethylene production, but via the fourelectron oxidation of 2-oxoglutarate to give ethylene in an argininedependent reaction. Crystallographic and biochemical studies on the Pseudomonas syringae ethylene-forming enzyme reveal a branched mechanism. In one branch, an apparently typical 2-oxoglutarate oxygenase reaction to give succinate, carbon dioxide, and sometimes pyrroline-5-carboxylate occurs. Alternatively, Grob-type oxidative fragmentation of a 2-oxoglutarate-derived intermediate occurs to give ethylene and carbon dioxide. Crystallographic and quantum chemical studies reveal that fragmentation to give ethylene is promoted by binding of L-arginine in a nonoxidized conformation and of 2-oxoglutarate in an unprecedented high-energy conformation that favors ethylene, relative to succinate formation.ethylene-forming enzyme | 2-oxoglutarate-dependent oxygenases | hydroxylase | plant development | oxidoreductase E thylene is of industrial importance and is a vital signaling molecule in plants, where it has roles in germination, senescence, and stress responses (1). Commercial manipulation of the natural ethylene response is agriculturally important in controlling fruit ripening (2). In higher plants, ethylene is produced from methionine, via oxidation of 1-aminocyclopropane-1-carboxylic acid (ACC) in an unusual reaction catalyzed by the Fe(II)-dependent ACC oxidase (ACCO) (3, 4), which is part of the 2-oxoglutarate (2OG)-dependent oxygenase superfamily, although it does not use a 2OG cosubstrate (Fig. 1A) (5-7). Ethylene is also produced in some microorganisms by oxidation of 2-oxo-4-methylthiobutyric acid in a reaction not directly enzyme catalyzed (8,9).In work aimed at producing industrial ethylene by biocatalysis, Pseudomonas strains, including plant pathogens, were shown to produce large amounts of ethylene (10)(11)(12)(13)(14). Bacteria engineered to produce ethylene using the Pseudomonas syringae pv. phaseolicola ethylene-forming enzyme (PsEFE) have been developed to ripen fruit as an alternative to the use of synthetic ethylene (15, 16). Ethylene-forming enzymes are being explored for biocatalysis in cyanobacteria (17-19). PsEFE-catalyzed ethylene production is 2OG-dependent and is stimulated by the addition of L-arginine (L-Arg), which is also converted by PsEFE into pyrroline-5-carboxylate (P5C; Fig. 1B) (13, 20). In contrast to the consensus 2OG oxygenase mechanism, which involves sequential binding of 2OG, substrate, and then oxygen, an unprecedented "dual circuit" mechanism is proposed for PsEFE (13).We describe biochemical, structural, and modeling studies supporting a branched mechanistic pathway for PsEFE that can lead either to ethylene via oxidative fragmentation of 2OG or to succinate via a more typical 2OG oxygenase reaction, which sometimes results in P5C formation (Fig....

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Structural and stereoelectronic insights into oxygenase-catalyzed formation of ethylene from 2-oxoglutarate

Zhang

Smart

Choi

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

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“…In these two organisms, a single ethylene forming enzyme (EFE) catalyses a complex set of two oxygen dependent reactions, i.e. formation of ethylene and succinate from 2-oxoglutarate and arginine [8], with concomitant formation of the by-products carbon dioxide, guanidine, and L- 1 -pyrroline-5-carboxylate (P5C).…”

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Flux balance analysis for ethylene formation in genetically engineered Saccharomyces cerevisiae

et al. 2011

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Biosynthesis of ethylene (ethene) is mainly performed by plants and some bacteria and fungi, via two distinct metabolic routes. Plants use two steps, starting with Sadenosylmethionine, while the ethylene-forming microbes perform an oxygen dependent reaction using 2-oxoglutarate and arginine. Introduction of these systems into Saccharomyces cerevisiae was studied in silico. The reactions were added to a metabolic network of yeast and flux over the two networks was optimized for maximal ethylene formation. The maximal ethylene yields obtained for the two systems were similar in the range of 7-8 mol ethylene/10 mol glucose. The microbial metabolic network was used for testing different strategies to increasing the ethylene formation. It was suggested that supplementation of exogenous proline, using a solely NAD-coupled glutamate dehydrogenase, and using glutamate as the nitrogen source, could increase the ethylene formation. Comparison of these in silico results with published experimental data for yeast expressing the microbial system confirmed an increased ethylene formation when changing nitrogen source from ammonium to glutamate. The theoretical analysis methods indicated a much higher maximal yield per glucose for ethylene than was experimentally observed.However, such high ethylene yields could only be obtained with a concomitant very high respiration (per glucose). Accordingly, when ethylene production was optimized under the additional constraint of restricted respiratory capacity (i.e. limited to experimentally measured values) the theoretical maximal ethylene yield was much lower at 0.2 mol/10 mol glucose, and closer to the experimentally observed values.

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NonhemeFe(II)‐ and 2‐Oxoglutarate‐Dependent Ethylene‐Forming Enzyme

Hausinger

Herr

2019

Encyclopedia of Inorganic and Bioinorganic Chemistry

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The ethylene‐forming enzyme (EFE) is a ferrous ion‐ and l ‐arginine ( l ‐Arg)‐dependent oxygenase that cleaves three carbon–carbon bonds of 2‐oxoglutarate (2OG) as it forms ethylene plus three molecules of carbon dioxide/bicarbonate. The enzyme also catalyzes the oxidative decarboxylation of 2OG (producing carbon dioxide and succinate) while hydroxylating the C5 position of l ‐Arg, with this intermediate species decomposing spontaneously to guanidine and L‐Δ‐1‐pyrroline‐5‐carboxylate. This secondary reaction is typical of the hydroxylation reactions catalyzed by a broad range of Fe(II)/2OG‐dependent oxygenases, whereas the ethylene‐generating reaction is unprecedented. Genes encoding homologs of EFE are present in specific fungi and bacteria, and the protein is proposed to be a virulence factor in some plant pathogens. The EFE sequence and structure are clearly related to those of 1‐aminocyclopropane‐1‐carboxylate oxygenase, an Fe(II)‐ and dioxygen‐dependent ethylene‐forming enzyme that does not require or utilize 2OG. By contrast, the EFE sequence is not significantly related to three Fe(II)/2OG‐dependent oxygenases (VioC, NapI, and OrfP) that catalyze other reactions with l ‐Arg (hydroxylation at C3, C4‐C5 desaturation, and C3,C4 dihydroxylation, respectively). The best characterized EFE is that from Pseudomonas syringae pv. phaseolicola strain PK2. A visible absorption spectrum associated with the Fe(II)/2OG metal‐to‐ligand charge‐transfer transition of EFE·Fe(II)·2OG is less intense than for other members of this enzyme family; this result is explained by the predominantly monodentate metal coordination of 2OG as seen in the corresponding EFE·Mn(II)·2OG crystal structure. Binding of l ‐Arg leads to an intensification of the Fe(II)/2OG visible absorption spectrum and a shift to bidentate metal coordination. In EFE·Mn(II)·2OG, the metal is bound by one oxygen atom of the Asp191 carboxylate, but in EFE·Mn(II)·2OG,· l ‐Arg this atom shifts to interact with l ‐Arg and the other carboxylate oxygen atom binds the metal. A reorientation of Tyr192 accompanies l ‐Arg binding, forming a hydrogen bond between the phenol hydroxyl group and the amino acid. The carboxylate shift and the aromatic side chain reorientation lead to a twisted Asp191‐Tyr192 peptide bond. The environment of 2OG in EFE is more hydrophobic compared to other family members. In combination, the altered position of the metal‐binding carboxylate, the twisted peptide bond, and the hydrophobic environment surrounding 2OG may all contribute to the ability of EFE to catalyze ethylene formation.

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Two reactions are simultaneously catalyzed by a single enzyme: The arginine-dependent simultaneous formation of two products, ethylene and succinate, from 2-oxoglutarate by an enzyme from Pseudomonas syringae

Cited by 88 publications

References 6 publications

Structural and stereoelectronic insights into oxygenase-catalyzed formation of ethylene from 2-oxoglutarate

Structural and stereoelectronic insights into oxygenase-catalyzed formation of ethylene from 2-oxoglutarate

Flux balance analysis for ethylene formation in genetically engineered Saccharomyces cerevisiae

NonhemeFe(II)‐ and 2‐Oxoglutarate‐Dependent Ethylene‐Forming Enzyme

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