Catalysis of nitrosyl transfer by denitrifying bacteria is facilitated by nitric oxide

Goretski, J; Hollocher, Thomas C.

doi:10.1016/0006-291x(91)91650-2

Cited by 15 publications

(6 citation statements)

References 30 publications

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“…These particular properties of NO could explain many of the biological responses in plants that have not been clearly understood yet, among them iron nutrition. A mechanism has already been described involving the oxidative activation of NO (Goretski and Hollocher, 1991). Besides, the anionic form (NO Ϫ ) can also react with Fe(III), analogous to the reaction of NO · with Fe(III).…”

Section: Discussionmentioning

confidence: 99%

Nitric Oxide Improves Internal Iron Availability in Plants

2002

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Iron deficiency impairs chlorophyll biosynthesis and chloroplast development. In leaves, most of the iron must cross several biological membranes to reach the chloroplast. The components involved in the complex internal iron transport are largely unknown. Nitric oxide (NO), a bioactive free radical, can react with transition metals to form metal-nitrosyl complexes. Sodium nitroprusside, an NO donor, completely prevented leaf interveinal chlorosis in maize (Zea mays) plants growing with an iron concentration as low as 10 m Fe-EDTA in the nutrient solution. S-Nitroso-N-acetylpenicillamine, another NO donor, as well as gaseous NO supply in a translucent chamber were also able to revert the iron deficiency symptoms. A specific NO scavenger, 2-(4-carboxy-phenyl)-4,4,5,5-tetramethylimidazoline-1-oxyl-3-oxide, blocked the effect of the NO donors. The effect of NO treatment on the photosynthetic apparatus of iron-deficient plants was also studied. Electron micrographs of mesophyll cells from iron-deficient maize plants revealed plastids with few photosynthetic lamellae and rudimentary grana. In contrast, in NO-treated maize plants, mesophyll chloroplast appeared completely developed. NO treatment did not increase iron content in plant organs, when expressed in a fresh matter basis, suggesting that root iron uptake was not enhanced. NO scavengers 2-(4-carboxy-phenyl)-4,4,5,5-tetramethylimidazoline-1-oxyl-3-oxide and methylene blue promoted interveinal chlorosis in iron-replete maize plants (growing in 250 m Fe-EDTA). Even though results support a role for endogenous NO in iron nutrition, experiments did not establish an essential role. NO was also able to revert the chlorotic phenotype of the iron-inefficient maize mutants yellow stripe1 and yellow stripe3, both impaired in the iron uptake mechanisms. All together, these results support a biological action of NO on the availability and/or delivery of metabolically active iron within the plant.Iron deficiency impairs chlorophyll biosynthesis and chloroplast development in both dicotyledonous and monocotyledonous species. Therefore, iron availability maintains a direct correlation with plant productivity. Chlorosis because of unavailability of iron in calcareous soils (high pH) is a major agricultural problem that results in diminished crop yields in an estimated 30% of calcareous soils worldwide (Mori, 1999).Iron deficiency responses involve several physiological plant adaptations (Guerinot and Yi, 1994;Mori, 1999). Under iron deficiency, plants have evolved two separate strategies for iron acquisition. Non-graminaceous plants (strategy I) enhance acidification of the extracellular medium and increase both root ferric-reducing capacity and uptake of ferrous iron. In contrast, graminaceous plants possess the ability to secrete phytosiderophores to enhance iron uptake from soils (strategy II). However, when iron availability is under a threshold level, both strategies I and II are not sufficient to support the iron requirement for plant development, and stress symptoms beco...

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Section: Discussionmentioning

confidence: 99%

Nitric Oxide Improves Internal Iron Availability in Plants

2002

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“…It was also shown that the extent of the 0-atom exchange reaction depended on the availability of electrons. The dependence of nitrosyl transfer upon the presence of NO during reduction of N02-has been demonstrated (11).…”

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Mutants of Pseudomonas fluorescens deficient in dissimilatory nitrite reduction are also altered in nitric oxide reduction

Arunakumari

Averill

et al. 1992

J Bacteriol

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Five Tn5 mutants of Pseudomonas fluorescens AK-15 deficient in dissimilatory reduction of nitrite were isolated and characterized. Two insertions occurred inside the nitrite reductase structural gene (nirS) and resulted in no detectable nitrite reductase protein on a Western immunoblot. One mutant had TnS inserted inside nirC, the third gene in the same operon, and produced a defective nitrite reductase protein. Two other mutants had insertions outside of this nir operon and also produced defective proteins. All of the Nir-mutants characterized showed not only loss of nitrite reductase activity but also a significant decrease in nitric oxide reductase activity. When cells were incubated with '5NO in H2180, about 25% of the oxygen found in nitrous oxide exchanged with H20. The extent of exchange remained constant throughout the reaction, indicating the incorporation of 180 from H218O reached equilibrium rapidly. In all nitrite reduction-deficient mutants, less than 4% of the '8O exchange was found, suggesting that the hydration and dehydration step was altered. These results indicate that the factors involved in dissimilatory reduction of nitrite influenced the subsequent NO reduction in this organism.Dissimilatory reduction of nitrite is the key step in the denitrification pathway; it is the point of divergence from assimilatory nitrogen metabolism (24). There are two types of nitrite reductases: one contains the cytochromes cdl, and the other contains copper (6,14,20). Organisms containing the cytochrome cd, nitrite reductases are more frequently isolated from nature, whereas Cu-type nitrite reductases are found in organisms that exhibit more phylogenic diversity and occupy a wider range of ecological niches (6, 9).Nitric oxide is the major product of nitrite reduction by purified nitrite reductases, and nitrous oxide is a minor product (4,14,17,26). NO is generally accepted as one of the free and obligatory intermediates in the denitrification pathway (2,5, 8,10,14,20,28), and NO reductases have been purified from Pseudomonas stutzeri Zobell (13) and Paracoccus denitnificans (4, 7). We recently showed that many denitrifiers containing Cu or cdl nitrite reductases are capable of undergoing 0-atom exchange with H2180 during the reduction of NO to N20 (27) and that a labeled intermediate can be trapped with azide. These results suggest that a nitrosyl complex is formed during the reaction. It was also shown that the extent of the 0-atom exchange reaction depended on the availability of electrons. The dependence of nitrosyl transfer upon the presence of NO during reduction of N02-has been demonstrated (11).TnS was used by Zumft et al. (29) to generate mutants deficient in dissimilatory nitrite reduction (Nir-) in P. stutzeri Zobell. All of the mutants isolated possessed normal NO reduction activity, indicating that NO reduction and nitrite reduction are distinct. The nitrite reductase gene (nirS) from Pseudomonas aeruginosa (21) and from two strains of P. stutzeri (Zobell [15]

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“…The generation of the single 14 N 15 NO product when the Fe− 15 NO reagent is used, but both 14 N 15 NO and 14 N 14 NO when the Ru− 15 NO reagent is used, suggests different intermediates. The Fe case is reminiscent of the products obtained when azide reacts with cyt cd 1 18,19 or nitroprusside, 33 and strongly suggests an intermediate of the form "Fe− 15 N-(=O)NNN" containing a coordinated linear nitrosyl azide. 34,35 In contrast, the generation of both 14 N 15 NO and 14 N 2 O in the case of Ru suggests an intermediate with a cyclic N 4 O contribution that decomposes via the two paths shown in Figure 5, where cleavage of bonds 1 and 3 in this intermediate would generate the unlabeled 14 N 2 O, whereas cleavage of bonds 3 and 5 would generate the singly labeled 14 N 15 NO.…”

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“…17 In the observed heme-based nitrosations, the active nitrosating intermediates in these cyt cd 1 enzymes are proposed to be the electrophilic [Fe 3+ −NO ↔ Fe 2+ −NO + ] species. 18,19 Interestingly, related nitrosations of C-based, Nbased, and S-based organics have been demonstrated in vitro for the muscle protein myoglobin. 20 It has been difficult to probe these heme-based nitrosation reactions, in large part due to the presumed instability of synthetic ferric-NO hemes.…”

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“…This is somewhat surprising, given the fact the cytochrome cd 1 enzymes from denitrifying and nondenitrifying bacteria have been shown to catalyze, using nitrite, the nitrosation of organics such as morpholine in vitro and in vivo to generate carcinogenic nitroso compounds. , Such heme-based nitrosations during bacterial infections have been postulated to contribute toward some cancers in animals and humans . In the observed heme-based nitrosations, the active nitrosating intermediates in these cyt cd 1 enzymes are proposed to be the electrophilic [Fe 3+ –NO ↔ Fe 2+ –NO + ] species. , Interestingly, related nitrosations of C-based, N-based, and S-based organics have been demonstrated in vitro for the muscle protein myoglobin …”

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Carbon–Nitrogen and Nitrogen–Nitrogen Bond Formation from Nucleophilic Attack at Coordinated Nitrosyls in Fe and Ru Heme Models

2017

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The conversion of inorganic NO species to organo-N compounds is an important component of the global N-cycle. Reaction of a C-based nucleophile, namely the phenyl anion, with the ferric heme nitrosyl [(OEP)Fe(NO)(5-MeIm)] generates a mixture of the C-nitroso derivative (OEP)Fe(PhNO)(5-MeIm) and (OEP)Fe(Ph). The related reaction with [(OEP)Ru(NO)(5-MeIm)] generates the (OEP)Ru(PhNO)(5-MeIm) product. Reactions with the N-based nucleophile diethylamide results in the formation of free diethylnitrosamine, whereas the reaction with azide results in NO formation; these products derive from attack of the nucleophiles on the bound NO groups. These results provide the first demonstrations of C-N and N-N bond formation from attack of C-based and N-based nucleophiles on synthetic ferric-NO hemes.

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Catalysis of nitrosyl transfer by denitrifying bacteria is facilitated by nitric oxide

Cited by 15 publications

References 30 publications

Nitric Oxide Improves Internal Iron Availability in Plants

Nitric Oxide Improves Internal Iron Availability in Plants

Mutants of Pseudomonas fluorescens deficient in dissimilatory nitrite reduction are also altered in nitric oxide reduction

Carbon–Nitrogen and Nitrogen–Nitrogen Bond Formation from Nucleophilic Attack at Coordinated Nitrosyls in Fe and Ru Heme Models

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