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1 Soil Biol. Biochem. Vol. 20, No. 6, pp , 1988 Printed in Great Britain. l rights reserved $ Copyright 1988 Pergamon Press pic SULPHUR-CONTAINING AMINO ACID METABOLISM IN SURFACE HORIZONS OF A HARDWOOD FOREST J. W. FITZGERALD and D. D. HALE Department of Microbiology, University of Georgia, Athens, GA 30602, U.S.A. and W. T. SWANK United States Department of Agriculture, Forest Service, Southeastern Forest Experiment Station, Otto, NC 28763, U.S.A. (Accepted 10 March 1988) Summary The, and horizons of a hardwood forest mineralized and incorporated into organic matter 35 S-labelled cysteine and methionine. Based upon assays of samples collected seasonally during 1 yr (n = 10-30), mineralization was the dominant process for cysteine whereas with methionine the reverse was true, except in the horizon. Analysis of samples for existing amounts of organic S revealed that carbon-bonded S was a major component throughout the sampling period in all horizons. This S pool was fractionated further into sulphonate S and amino acid S. The former component represented, on a mean annual basis, 59, 44 and 28% of total S in the, and horizons, respectively. In contrast, amino acid S comprised 22, 24 and 15% of the total S in these respective horizons. With horizon samples, decreases in existing amounts of amino acid S coincided with increases in cysteine mineralization suggesting that cysteine is an important component of this S pool in the horizon. INTRODUCTION In addition to anthropogenic inputs of sulphate (Likens and Bormann, 1974), the mineralization of organic S may represent an equally important source of sulphate for hardwood forests. Carbon-bonded S, a component of this S pool, is a major constituent of leaves and it might be anticipated that large quantities of it enter soil during deciduous senescence. This form of S is comprised of organic sulphonates and the S-containing amino acids, methionine and cysteine. The sulphonate linkage is found in the sulphoquinovose component of the plant sulpholipid which, as the nomenclature implies, has a widespread occurrence in photosynthetic as well as nonphotosynthetic tissues (Harwood and Nicholls, 1979; Harwood, 1980). Strickland and Fitzgerald (1983) and Fitzgerald and Andrew (1984) demonstrated that sulphoquinovose S and methionine S were rapidly converted to sulphate during incubation with hardwood forest litter and soil. Moreover, a portion of the released sulphate S could only be recovered by acid and base extraction, suggesting that the anion had been incorporated into organic matter in a manner analogous to that observed when sulphate was added directly to litter and soil from the same forest (Fitzgerald et al., 1982; Strickland and Fitzgerald, 1985). Unlike results obtained with sulphoquinovose, a portion of the methionine added to samples was also recovered by acid extraction suggesting that this amino acid can also be incorporated into organic matter presumably via the formation of acid-labile peptide bonds (Fitzgerald et al., 1984). Support for this possibility was obtained (Watwood and Fitzgerald, unpublished) when it was shown that organic matter could be extracted without significant loss of radioactivity S.B.B. 206 D 825 after incubation of soil with 35 S-labelled methionine. Release of the amino acid was achieved chemically only by treatment with strong acid or base. This additional metabolic fate of immobilization for methionine may govern the availability of the amino acid for mineralization after release during deciduous senescence. In order to evaluate the importance of amino acid S as a source of sulphate for hardwood forests, we have compared, on a seasonal basis, in situ amounts of this form of S to those of other forms of organic S in, and horizon samples. Attempts have also been made to correlate intrinsic amounts of amino acid S to laboratory-derived potentials for the mineralization and incorporation into organic matter of both methionine and cysteine. MATERIALS AND METHODS Sample collection Three random samples from the forest floor ( and layers) and the horizon (0-5 cm) were collected from each of 10 permanent plots on watershed at the Coweeta Hydrologic Laboratory, located near Otto, N.C. The plots, characterized by differing vegetation, are located on a ridge-to-streamto-ridge transect of this catchment (Swank et al., 1984). Watershed is a mixed mature hardwood forest with soils of the sandy loam Ashe series, a Typic Dystrochrept. To observe seasonal patterns, litter and soil were collected in May, July and November 1984 and February and May Samples were stored (field moist) in sealed polyethylene bags at 10 C before analysis following sieving (<1 cm) to remove small roots and stones.
2 826 J. W. FITZGERALD et al. Mineralization and immobilization of 35 S-labelled amino acids Samples (0.5g 01, 02 and l.og soil, wet wt) were held for 24 h at 30 C with 8.4nmol of either L-methionine or L-cysteine (mixture of unlabelled and 35 S-labelled amino acid). Following addition of the amino acid, water (10il) was added to each sample to ensure even distribution of the label. After incubation, samples were extracted with 1 M Na 2 SO 4 in a saturated solution of the appropriate unlabelled amino acid followed by 2 washes with a saturated solution of the amino acid alone. This treatment effectively terminated by isotope dilution further release of 35 S-sulphate or incorporation of 35 S-amino acids. The samples were then washed 3 times each with 1 M NaH 2 PO 4, LiCl and water. l fractions, which were combined to yield a salt extract, contained soluble and adsorbed sulphate produced by mineralization in addition to non-metabolized amino acid. The extract was kept at 20 C until analyzed by electrophoresis. Some of the 35 S incorporated by the samples into organic matter was recovered after hydrolysis of the residue in 6M HC1 for 12 h at 121 C followed by 3 water washes. These fractions were combined to yield an acid extract maintained as described above. The 35 S remaining in the samples was obtained by extraction with 2 M NaOH followed by 3 water washes. Once again the fractions were combined to yield a base extract which was stored as above. Irrespective of the amino acid studied, between 85 and 95% of the added 35 S was recovered by this salt, acid and base extraction sequence. Banwart and Bremner (1975) found that S present in methionine or cysteine was volatilized when these amino acids were incubated with soil for 40 days at 30 C. In related work (Banwart and Bremner, 1976), added sulphate-s was not converted to volatile forms to any significant extent. though similar recoveries of added label are obtained routinely when samples from this watershed were incubated with sulphate (Fitzgerald et al., 1982), our failure to achieve complete recovery of 35 S in this instance may be attributed in part to volatilization of amino acid S. Further work supporting the efficacy of this extraction procedure, similar to that of Houghton and Rose (1976), is described by Fitzgerald et al. (1984). Electrophoresis Radioactive components in each extract were separated by electrophoresis on Whatman No. 1 paper for 2h at 250V in a 0.1 M barium acetate-acetic acid buffer, ph 4.5. In this buffer system, inorganic sulphate precipitates as BaSO 4 at the origin while other components move away from it. Radioactive components were located on dried paper strips by scanning with a Packard Radioelectrophoretogram Scanner. Typical scans observed with extracts from soil samples incubated with 35 S-methionine are available (Fitzgerald and Andrew, 1984). The amount of radioactivity associated with each component was determined by triangulation of the peak corresponding to it. The radioactivity thus calculated for each component was expressed as a percentage of the total radioactivity of the extract determined by counting a 20^1 subsample in 5ml ScintiVerse (Fisher) with a scintillation counter. The amount of each component was then calculated from the amount of 35 S added and was standardized to a 1 g dry wt basis to allow comparison of samples with differing moisture content. The potential for mineralization of each amino acid was calculated from the amount of 35 S-sulphate present in the salt, acid and base extracts while the potential for amino acid incorporation into organic matter was determined from the amount of 35 S-amino acid present in acid and base extracts. Determination of intrinsic S pool sizes Total S was determined by hydriodic acid (HI) reduction of samples following alkaline oxidation with hypobromite (Tabatabai and Bremner, 1970). Hydriodic acid-reducible S, consisting of ester sulphate and inorganic sulphate, was determined by direct sample reduction with this acid (Freney, 1961). Raney nickel reduction (Freney et al., 1970) was used to quantify amino acid S. Total carbon-bonded S was calculated as the difference between total S and Hi-reducible S while sulphonate S was determined as the difference between carbon-bonded S and amino acid S. Ester sulphate was calculated as the difference between total Hi-reducible S and inorganic sulphate. The latter was obtained by shaking 4 g (wet wt) of each sample with 20 ml water for 15 min followed by centrifugation and removal of the supernatant. This fraction, containing soluble sulphate, was retained while the pellet was resuspended in and shaken with 20ml of 50 mm Na,HPO 4 for 30 min to recover adsorbed sulphate. Following centrifugation and collection of the supernatant, the residue was again extracted with 20 ml of 50 mm Na,HPO 4. Inorganic sulphate present in these combined fractions was determined by ion chromatography (Dick and Tabatabai, 1979). Statistical analysis Data from all analyses were assessed by 2-way analysis of variance and Duncan's multiple range test. RESULTS AND DISCUSSION Metabolism of 35 S-labelled amino acids Three major radioactive components generated by incubation of litter and soil with 35 S-cysteine were observed on electrophoretograms. These included sulphate, nonmetabolized cysteine (determined by co-electrophoresis with an authentic standard) and trace quantities of a cysteine oxidation product having a mobility similar to that of cysteic acid. The latter appeared at the same position as the dominant peak on electrophoretograms of a 35 S-cysteine stock solutin treated with base. Typically, the oxidation product appeared only on electrophoretograms of base extracts, suggesting that oxidation may have occurred either before incorporation or after the release of cysteine from organic matter. Likewise, four major radioactive components from the incubation of litter and soil with 35 S-methionine were observed on electrophoretograms. These included
3 Sulphur metabolism 827 Table 1. Incorporation into organic matter of sulphate-s generated from amino acid mineralization 11 Sulphate recovered by acid and base extraction (nmol S g ' dry wt + SE) Amino acid Cysteine Methionine Horizon July (0.6) 3.6 (0.2) 0.7 (0.04) 10.6(1.4) 8.1 (1.0) 1.5(0.1) Nov (0.8) 7.6 (0.5) 1.9(0.1) 4.3 (0.5) 9.5(0.6) 2.1 (0.07) Feb (0.2) 7.8 (0.5) 2.0 (0.09) 4.5(0.5) 3.1(0.1) 1.6(0.05) May (0.1) 2.9(0.3) 1.8(0.1) 0.8(0.1) 2.4(0.3) 1.4(0.07) 'Samples were collected from all 10 plots on watershed in (he indicated months and incubated with cysteine or methionine. Amounts of sulphate present in acid and base extracts were determined from electrophoretograms of these extracts, n = 10. sulphate, nonmetabolized methionine and two methionine oxidation products, tentatively identified as methionine sulphoxide and methionine sulphone (Fitzgerald and Andrew, 1985). As with cysteine, the oxidation products of methionine tended to appear only in the base extracts. The presence of the amino acids (and oxidation products) in acid and base extracts indicated that the amino acids had been incorporated into organic matter during incubation. The presence of sulphate in all extracts indicated that the amino acids had been mineralized and, in the case of the acid and base extracts, that some sulphate-s had been incorporated into organic matter. The amount of sulphate present in these combined extracts of samples collected from all horizons during 1 yr is shown in Table 1. Mineralization potentials reported in this work are therefore based on 35 S-sulphate recovered by acid-base as well as salt and water extraction.. Table 2 shows potentials for mineralization and incorporation into organic matter of cysteine and methionine by, and horizon samples. In each horizon, the potential for cysteine mineralization was always greater than the potential for incorporation of this amino acid whereas with methionine the opposite was true, except in the horizon. Mineralization potentials for both amino acids tended to be highest in the horizon, followed by the and horizons, respectively. Incorporation potentials for cysteine also followed this trend, but the potential for incorporation of methionine into organic matter tended to be highest in the horizon, followed by the and horizons, respectively. With respect to seasonal effects, Table 2 shows that, in most cases within a given horizon, potentials for mineralization and incorporation of either amino acid varied significantly. Cysteine transformation potentials were not significantly different in only two instances (eg. cysteine mineralization in the horizon in November 1984 and February 1985 and cysteine incorporation in the horizon in February and May 1985). However, with methionine, in 7 instances transformation potentials were not significantly different. In particular, the potential for methionine mineralization was not significantly different in samples collected from the horizon during 3 of the 4 sampling dates. Thus, although no definite trends were observed for either transformation potential, transformation potentials for cysteine showed more seasonal variability than those for methionine. Sulphur pool sizes and their relationship to amino acid transformation potentials On a dry weight basis, total S was higher in the forest floor than the soil in all seasons in which samples were collected (Table 3). With the exception of amounts in the horizon in May and July 1984, the amount of total S in the and horizons, respectively, differed significantly between sampling dates. In the horizon, however, total S remained constant throughout, with the exception of samples collected in May Carbon-bonded S was the major form of S in the forest floor, with sulphonate S rather than amino acid S comprising the major portion of this pool (Table 4). though carbon-bonded S did not dominate in the horizon, sulphonate S once again comprised a larger portion of total S than did amino acid S. In considering the amounts of amino acid S, Table 3 Transformation Cysteine mineralization Cysteine incorporation Methionine mineralization Methionine incorporation Table 2. Amino acid transformation potentials of litter and soil Mean potential (nmol S g 1 dry wt) and (±SE) a Horizon July 1984 Nov Feb (3.8)a 23.1 (3.4)b 13.4(1.6)c 40.6(2.6)a 46.1(2.0)b 46.6(3.2)b 5.9(0.3)a 11.2(0.30b 13.0(0.2) (0.9)a 13.7(2.1)b 3.6 (0.4)c 7.6(0.5)a 14.0(1.3)b 5.7 (0.8)c 1.0(0.04)a 1.5(0.1)b 0.6(0. l)c 23.8(2.6)a 9.3 (0.9)b 6.6 (0.7)c 26.8 (3. 3)a 19.0(1.5)b 7.2(0.5)c 5.5 (0.3)a 5.1 (0.2)b 5.8 (0.3)a 45.9 (4.4)a 26.4 (4. 1 )b 25.5(3.1)b 23.9 (2.6)a 31.5(2.0)b 8.7 (0.3)c 1.8(0.1)a 2.7(0.1)b 2.0(0. l)c "The mean of separate determinations on a sample taken from each of the 10 plots is reported (n followed by the same letter are not significantly different (P = 0.05). May (0.1)d.2(1.6)c 16.7(1.0)d 3.9 (0.2)c 4.7 (0.5)d 2.5 (0.2)d 1.6(0.3)d 7.1 (l.o)c 5.9 (0.4)a 13.0(1.0)c 9.1 (l.l)c 2.0(0.1)0 10). Within a given horizon, means
4 828 J. W. FITZGERALD el al. Sulphur form Total Amino acid HI-reducibIe b Sulphate Table 3. Sulphur forms and pool sizes in liter and soil Mean pool size (*g S g" 1 dry wt) and ( + SE) ;I Horizon May 1984 July 1984 Nov Feb May (202)a 1102(65)b 550 (35)c 1668(132)d 676 (23)e 1325(77)a 1303(45)a 1069(46)b 625(31)c 951 (39)d 295 (23)a 244(12)b 230 (6)b 232 (9)b 239 (4)b 270(21)a 359 (28)b 4(10)c 280 (69)a 56 (3)d 452(21)a 443 (20)a 219(15)b 108(7)c 155(8)d 69 (7)a 45 (4)b 29(2)c 25(1 )c (l)d 5(28)a 222(15)b 165(52)a 314(89)c 109(4)d 375 (26)a 415()b 6(19)c 230 (9)d 274(16)e 133(ll)a 130(5)a 157(7)c 143 (4)b 146(4)b NDa 23 (4)b 24(3)b 1 (2)c 14(2)c 15(3)a 175(29)b 31 (4)c 1 1 (2)a 12(2)a 19(5)a 70 (5)b 33 (3)c 23 (4)d 46 (7)e "For each horizon, the mean of triplicate determinations on samples from each of the 10 plots is reported (n =30), except for sulphate («= 10). Within a given horizon, means followed by the same letter are not significantly different (P = 0.05); ND, not detectable. b Hydriodic acid reducible. shows that significant differences were observed within each horizon for 4 of the 5 sampling periods. Thus, concentrations of amino acid S may be expected to fluctuate significantly on a seasonal basis. Hydriodic acid-reducible S was the major form of S in the horizon, with ester sulphate rather than inorganic sulphate comprising the major portion of this S form. As shown in Table 4, the dominance of ester sulphate over inorganic sulphate was also observed with and horizon samples, although hydriodic acid-reducible S was not the major S form in these samples. Significant differences in the amount of sulphate were observed more often with horizon samples than with the and horizons (Table 3). Fluctuations in potentials for mineralization of amino acids, those for cysteine in particular, may be a factor in explaining the differences observed in the amounts of inorganic sulphate in the horizon. Comparison of amino acid S pools at various sampling dates with amino acid S transformation potentials for the same samples revealed definite relationships. In the horizon (Fig. 1), the incorporation potential for cysteine and methionine together exceeded the combined mineralization potential for the amino acids irrespective of sampling date. Decreases in incorporation potentials for the amino acids, mainly that for methionine, were followed by decreases in amounts of amino acid S in the samples. In the horizon (Fig. 2), the combined mineralization potential for cysteine and methionine exceeded the combined incorporation potential. Mineralization of cysteine occurred to a greater extent than that of methionine, and increases in cysteine mineralization coincided with decreases in amino acid S content in the same samples. In the horizon, where mineralization of the amino acids again surpassed potentials for their incorporation into organic matter, increases in amino acid S mineralization potentials, mainly that of cysteine, were paralleled by decreases in amounts of amino acid-s in the samples (Fig. 3). The observation that metabolism of methionine was more closely correlated with existing amounts of amino acid S in horizon samples may be explained by the fact that the capacity for methionine incorporation in this horizon exceeded all other amino acid S transformation potentials. Likewise, the relationship between intrinsic amino acid S and the metabolism of cysteine in the and horizons may be explained by the fact that the capacity for mineralization of cysteine in these horizons exceeded all other amino acid S transformation potentials. In evaluating the importance of organic S as a source of sulphate for hardwood forests, these and other data (Strickland and Fitzgerald, 1983) suggest Sulphur form Carbon-bonded" Sulphonate b Amino acid Ester 0 Sulphate Table 4. Forms of sulphur in litter and soil as a percentage of total sulphur Sampling date Horizon May 1984 July 1984 Nov Feb "Total S minus total hydriodic acid (Hl)-reducible S. b Carbon-bonded S minus amino acid S. 'Total Hi-reducible S minus sulphate. May
5 Sulphur metabolism r~ UJ CO to w 250 I ^_ i i -I o CO 'o * o S >. 8 *.E T.ii o 5 N c I 12 n 2 0) C JUL'84 NOV'84 FEB'85 MAY'85 Fig. 1. Relationship between intrinsic amounts of amino acid S in the horizon and amino acid transformation potentials, 72 = 10. Reading from left to right, the figure shows amino acid S content (double hatches), mineralization potentials for methionine (medium dots), mineralization potentials for cysteine (single hatches) and incorporation potentials for these respective amino acids. that mineralization of carbon-bonded S may greatly influence sulphate concentrations. This was especially apparent in the and horizons, where this form of organic S was a major component. Because sulphoquinovose has been shown (Strickland and Fitzgerald, 1983) to be rapidly converted to sulphate as well as to ester sulphate which was in turn capable of being remineralized, generation of sulphate might be expected with other sulphonates, which were shown here to represent major components of the carbon-bonded S of these horizons. Work with random samples collected during Summer (Fitzgerald and Andrew, 1984; Fitzgerald et a., 1984) had suggested that methionine-s was a potential source of this anion for a number of watersheds in the Coweeta basin. However, the extent 45O UJ 300 CO CO O r- o.5 ' OT i 1'1 y T i, *; JL ^ ^ ^' '. 1 i ^ ; ^ i _ 30 ~ 24 - o OL.,.1 o Q ^ ^ JUL'84 ^ NOV'84 E 5. S 1 FEB'85 ; - 12 i i;ji 6 i ~ ^ i -I MAY'85 Fig. 2. Relationship between intrinsic amounts of amino acid S in the horizon and amino acid transformation potentials, n = 10 (see Fig. 1).
6 830 J. W. FITZGERALD ei al CQ) 36 _ 12 g_ LJ CO o CO CO -H 30 1,- ~ 10 o t! -o S i ex S 0 >> 24 i O C «- 8 o ^ o 1 ^ 'c CT c *- 1 0 I. CO " < OT en ~ i i a. i$ j; 6 c <D i.2 o s " a '. QJ c 6 - a xsj] - 2 i X XX L&HEra S Xx E ffl o ffl x ' i t : n JUL'84 NOV'84 FEB' 85 MAY 85 Fig. 3. Relationship between intrinsic amounts of amino acid S in the AI horizon and amino acid transformation potentials, n = 10 (see Fig. 1). x 16 of mineralization was regulated by incorporation of the amino acid into organic matter and by amino acid adsorption. Data from extensive sampling over 1 yr in the current study support these possibilities for the metabolic fate of both methionine and cysteine. though these amino acids were mineralized as well as incorporated into organic matter, the extent to which each process occurred determined the relative importance of the amino acid as a source of sulphate. Because the potential for mineralization was much greater than that for incorporation for cysteine, this amino acid may represent an important short-term source of sulphate in all horizons. The reverse was true in the case of methionine, suggesting that this amino acid may represent a long-term source of sulphate at least in the OI and horizons. Due to the higher mineralization potentials for cysteine as opposed to methionine in all horizons and the possibility that more cysteine than methionine occurs in soil from the study site as well as in other soils (Freney et al., 1972), cysteine probably serves as a more important overall source of sulphate. Finally, because amounts of amino acid S were lower than those for sulphonate S in all samples, cysteine and methionine may not be as important a source of sulphate as the sulphonates in this forest ecosytem. Acknowledgement This research was funded as part of the National Acid Precipitation Assessment Program by the U.S.DA, Forest Service, Southeastern Forest Experiment Station. REFERENCES Banwart W. L. and Bremner J. M. (1975) Formation of volatile sulfur compounds by microbial decomposition of sulfur-containing amino acids in soils. Soil Biology & Biochemistry 7, Banwart W. L. and Bremner J. M. (1976) Volatilization of sulfur from unamended and sulfate-treated soils. Soil Biology & Biochemistry 8, Dick W. A. and Tabatabai M. A. (1979) Ion chromatographic determination of sulfate and nitrate in soils. Soil Science Society of America Journal 43, Fitzgerald J. W. and Andrew T. L. (1984) Mineralization of methionine sulphur in soils and forest floor layers. Soil Biology & Biochemistry 16, Fitzgerald J. W. and Andrew T. L. (1985) Metabolism of methionine in forest floor layers and soil: influence of sterilization and antibiotics. Soil Biology & Biochemistry 17, Fitzgerald J. W., Andrew T. L. and Swank W. T. (1984) Availability of carbon-bonded sulfur for mineralization in forest soils. Canadian Journal of Forest Research 14, Fitzgerald J. W., Strickland T. C. and Swank W. T. (1982) Metabolic fate of inorganic sulphate in soil samples from undisturbed and managed forest ecosystems. Soil Biology & Biochemistry 14, Freney J. R. (1961) Some observations on the nature of organic sulphur compounds in soil. Australian Journal of Agricultural Research 12, Freney J. R., Melville G. E. and Williams C. H. (1970) The determination of carbon bonded sulfur in soil. Soil Science 109, Freney J. W., Stevenson F. J. and Beavers A. H. (1972) Sulfur-containing amino acids in soil hydrolysates. Soil Science 114, Harwood J. L. (1980) Sulfolipids. In The Biochemistry of Plants (P. K. Stumpf and E. E. Conn, Eds), Vol. 4, pp Academic Press, New York. Harwood J. L. and Nicholls R. G. (1979) The plant sulpholipid a major component of the sulphur cycle. Biochemical Society Transactions 1, Houghton C. and Rose F. A. (1976) Liberation of sulfate from sulfate esters by soils. Applied and Environmental Microbiology 31, Likens G. E. and Bormann F. H. (1974) Acid rain: a serious regional environmental problem. Science 4,
7 Sulphur metabolism 831 Strickland T. C. and Fitzgerald J. W. (1983) Mineralization Swank W. T., Fitzgerald J. W. and Ash J. T. (1984) of sulphur in sulphoquinovose by forest soils. Soil Microbial transformation of sulfate in forest soils. Science Biology & Biochemistry 15, , 2-4. Strickland T. C. and Fitzgerald J. W. (1985) Incorporation Tabatabai M. A. and Bremner J. M. (1970) An alkaline of sulphate-sulphur into organic matter extracts of litter oxidation method for determination of total sulfur in and soil: involvement of ATP sulphurylase. Soil Biology soils. Soil Science Society of America Proceedings, & Biochemistry 17, 779^
Soil B/o/. Biochem. Vol. 20, No. 6, pp , 1988 Printed in Great Britain. All rights reserved
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