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Microbial Assimilation of Ammonium (L-Methionine Sulfoximine/Glutamine/Asparagine) GREGORY W

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Microbial Assimilation of Ammonium (L-Methionine Sulfoximine/Glutamine/Asparagine) GREGORY W Proc. Nati. Acad. Sci. USA Vol. 89, pp. 453-456, January 1992 Agricultural Sciences Regulation of assimilatory nitrate reductase activity in soil by microbial assimilation of ammonium (L-methionine sulfoximine/glutamine/asparagine) GREGORY W. MCCARTY AND JOHN M. BREMNER* Department of Agronomy, Iowa State University, Ames, IA 50011-1010 Contributed by John M. Bremner, October 24, 1991 ABSTRACT It is well established that assimilatory nitrate MATERIALS AND METHODS reductase (ANR) activity in soil is inhibited by ammonium The soils used (Table 1) were surface samples (0-15 cm) of (NHIt). To elucidate the mechanism of this inhibition, we Iowa soils that had been sieved (2-mm screen) and stored studied the effect of L-methionine sulfoximine (MSX), an (4°C) in the field-moist condition. Immediately before use in inhibitor of NH' assimilation by microorganisms, on assimi- studies of assimilatory reduction of NO- by soil microorga- latory reduction ofnitrate (NO-) in aerated soil slurries treated nisms, subsamples of each soil were preincubated at 30°C for with NH:. We found that NHj strongly inhibited ANR activity 16 hr after treatment with glucose (2.5 mg of carbon per gram in these slurries and that MSX eliminated this inhibition. We of soil) to stimulate microbial activity and assimilation of also found that MSX induced dissimilatory reduction of NO3 preexisting NH' and NO-. They were then treated with to NHI in soil and that the NH$ thus formed had no effect on KNO3 (60 ,ug of nitrogen per gram of soil) and glucose (500 the rate of NO - reduction. We concluded from these observa- ,g of carbon per gram of soil) and shaken with water (3 ml/g tions that the inhibition of ANR activity by NHj is due not to of soil) to obtain slurries for the experiments reported. NH+ per se but to products formed by microbial assimilation To continuously monitor the effects of different treatments of This conclusion was supported by a study of the effects on ANR activity in soil by use of NO- electrodes, slurries NHI4. containing 10 g (dry weight) of soil were treated with 14 mg of early products of NH+ assimilation (L amino acids) on ANR of K2SO4 (added to adjust ionic strength), placed on magnetic activity in soil, because this study showed that the biologically stirrers in a room maintained at 30°C, and aerated by bubbling active, L isomers of glutamine and asparagine strongly inhib- with a stream of air. A NO3 electrode (Orion model 93-07) ited ANR activity, whereas the D isomers of these amino acids coupled with a double-junction reference electrode (Orion had little effect on ANR activity. Evidence that ANR activity is model 90-02) containing 0.4 M K2SO4 outer filling solution regulated by the glutamine formed by NH4: assimilation was was inserted into each slurry, and the millivolt output was provided by studies showing that inhibitors of glutamine me- continuously charted by a pen recorder connected to an tabolism (azaserine, albizziin, and aminooxyacetate) inhibited ion-selective electrode meter. At different times during in- ANR activity in soil treated with NO1 but did not do so in the cubation, soil slurries were treated with one or more of the presence of MSX. following amendments: 1.2 mg of nitrogen as (NH4)2SO4, 10 ,umol of L-methionine sulfoximine (MSX), 100 ,mol of D- or There is international concern about the potential adverse L-glutamine or D- or L-asparagine, 10 kimol of azaserine, 45 effects of fertilizer-derived nitrate (NO-) on environmental ,umol of aminooxyacetate, and 68 ,umol of albizziin. quality and public health (1-4). This concern has stimulated To study the effect of MSX on NO reduction and NH' research on the biological and nonbiological processes that production in soil, slurries containing 40 g (dry weight) of soil, affect the fate of NO3 in soils, and it is well established that 2.4 mg of nitrogen as KNO3, and 20 mg of carbon as glucose NO- is the substrate of at least three microbial processes in were treated with 0 or 40 izmol of MSX and shaken at 30°C. soils: denitrification, assimilatory NO- reduction, and dis- Aliquots (5 ml) of slurry were taken at 40-min intervals, reduction mixed with 5 ml of 4 M KCl, filtered through Whatman no. similatory NO- reduction. Denitrification leads to 5 filter paper, and analyzed colorimetrically for NH' and of NO- to dinitrogen (N2) and nitrous oxide (N20), whereas NO- by flow injection analysis (Lachat Instruments, Mil- both assimilatory and dissimilatory NO- reduction lead to waukee). The same experiments were performed using conversion of NO3 to NH'. Dissimilatory NO- reduction is KNO3 containing 1.0 atom % '5N to confirm that the NH'4 not affected by NH' (5), whereas assimilatory NOj reduc- produced by incubation of the soil slurries was derived from tion is strongly inhibited-by NH' (6). the NOj added. In these tracer experiments, aliquots of the It is generally assumed that assimilatory NO- reduction is filtrates used for NH4 and NOj analysis were analyzed as a minor fate of NO- in soil compared with plant uptake, described by Bremner (12) to determine the N-isotope ratios leaching, and denitrification (7-9). This assumption is based of these forms of nitrogen. largely on studies showing that NH' is a potent inhibitor of MSX, azaserine, albizziin, aminooxyacetate, and D and L NO- assimilation by soil microorganisms and that NH' isomers of glutamine and asparagine were obtained from concentrations in agricultural soils are usually greater than Sigma. The other chemicals used were obtained from Fisher those required to inhibit assimilatory NO- reductase (ANR) Scientific. activity (9-11). Very little information is available, however, concerning assimilatory reduction of NO- in soil and the factors affecting this process. The purpose of the work RESULTS AND DISCUSSION reported here was to elucidate the mechanism of inhibition of To investigate the role of NH' assimilation in regulation of ANR in soil by NH't. ANR activity in soil, we studied the effect of MSX, an The publication costs of this article were defrayed in part by page charge Abbreviations: ANR, assimilatory nitrate reductase; MSX, L-me- payment. This article must therefore be hereby marked "advertisement" thionine sulfoximine. in accordance with 18 U.S.C. §1734 solely to indicate this fact. *To whom reprint requests should be addressed. 453 Downloaded by guest on October 2, 2021 454 Agricultural Sciences: McCarty and Bremner Proc. Nati. Acad. Sci. USA 89 (1992) Table 1. Properties of soils used not by ammonification of organic nitrogen. These observa- Organic Total tions indicate that dissimilatory reduction ofNO- to NH' in Soil carbon, nitrogen, Sand, Clay, CCE,t soil can occur via ANR activity under conditions that inhibit Series Subgroup* pH % % % % % assimilation of NH'. Harps TC 7.9 4.2 0.50 9 43 41 The experiments reported in Figs. 1 and 2 indicate that the Okoboji CH 7.1 2.8 0.22 19 34 0 observed inhibition of ANR activity in soil by NH' was due not to NH' per se but to products formed by microbial *TC, Typic Calciaquoll; CH, Cumulic Haplaquoll. assimilation of NH'. This conclusion was supported by a tCCE, CaCO3 equivalent. study of the effects of glutamine and asparagine (early inhibitor of NH' assimilation by microorganisms, on ANR products of NH' assimilation) on ANR activity in soil, activity in aerated soils treated with NH'. We found that because this study showed that the biologically active, L MSX eliminated the inhibitory effect of NH' on ANR isomers of these amino acids markedly inhibited ANR activ- activity in the soils studied and that its influence on this ity, whereas the D isomers had little effect on ANR activity inhibition was not dependent on the order ofaddition ofNH'4 (Table 2). and MSX (Fig. 1). We also found that MSX induced dissim- Previous workers (9) concluded that NH' inhibition of ilatory reduction ofNO- to NH' in aerated soils treated with ANR activity in soil was not dependent on assimilation of NOQ and that the NH' thus formed did not affect the rate of NH' by soil microorganisms. This conclusion was based NO- reduction (Fig. 2). Studies using "N-labeled NO- largely on the observation that inhibition of ANR activity by showed that most (>90%o) of the NH' formed in these NH' was considerably more rapid than the corresponding experiments was produced from NO- by ANR activity and inhibition by amino acids known to be formed by assimilation Harps 65 r 65 r 65 60 60 60 -4 0 55 55 55 NH4 NH4 MSX 0 tobO 50 / 50 [ /1 50 . 45 45 45 4) 0 4 40 40 40 35 35 k 35 zO 30 _ 30 F 30 , 25 _, 25 I 25 0 30 60 90 120 0 30 60 90 120 0 30 60 90 120 Time, min Time, min Time, min Okoboji 65r 65 r 65 r 60 60 60 -4 MSX cW0 55 55 55 k '4-I 0to Z 50 50 50 k NII4 r 45 45 _ 45 bo .-0 4 40 _ 40 35 _ 35 z 30 30 k 30 k 25 25 25 Il h h 0 30 60 90 120 0 30 60 90 120 0 30 60 90 120 Time, min Time, min Time, min FIG. 1. Effect of MSX on NH' inhibition of ANR activity in Harps and Okoboji soil. Slurries containing 10 g (dry weight) of soil, 30 ml ofwater, 0.6 mg of KNO3 nitrogen, 5 mg ofglucose carbon, and 14 mg of K2SO4 were incubated at 30°C and treated with 1.2 mg of NH' nitrogen and 0 or 10 ,umol of MSX at the times indicated.
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