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Soil Science Society of America Journal 63:1188-1198 (1999)
© 1999 Soil Science Society of America

DIVISION S-3-SOIL BIOLOGY & BIOCHEMISTRY

Bacterial and Fungal Cell-Wall Residues in Conventional and No-Tillage Agroecosystems

Georg Guggenbergera, Serita D. Freyb, Johan Sixc, Keith Paustianc and Edward T. Elliottc

a Lehrstuhl für Bodenkunde und Bodengeographie, Universität Bayreuth, 95440 Bayreuth, Germany
b School of Natural Resources, 2021 Coffey Road, Ohio State University, Columbus, OH 43210-1085 USA
c Natural Resource Ecology Lab., Colorado State Univ., Fort Collins, CO 80523 USA

georg.guggenberger{at}uni-bayreuth.de


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 Materials and methods
 Results
 Discussion
 Conclusions
 REFERENCES
 
Agricultural management practices have been shown to influence the decomposer community in soils, with no-tillage (NT) systems favoring fungi as compared with conventional tillage (CT) systems. In this study, we examined six North American agroecosystems with respect to the effects of NT vs. CT management systems on the accrual of microbial cell-wall residues in surface soil. We used total amino sugar contents to estimate living and decomposing microbial cell-wall mass in soil and the contents of glucosamine and muramic acid to separate fungal and bacterial contributions to microbial-derived soil organic matter (SOM). Compared with estimates of glucosamine and muramic acid present in living biomass of fungi and bacteria, total concentrations of these compounds (745–2076 mg glucosamine kg-1 soil and 37–79 mg muramic acid kg-1 soil) were larger by factors of 54 to 745 and 26 to 82, respectively. At three sites, the ratios of glucosamine to muramic acid in NT soils (32.0, 30.0, 42.2) significantly exceeded those in the respective CT soils (18.8, 22.1, 23.0) because of a higher enrichment of glucosamine. This coincided with higher values for fungal biomass, particulate organic matter carbon (POM-C), mean weight diameter of water-stable aggregates (MWD), and total organic carbon (TOC). Analysis of aggregate-size classes showed that the additional glucosamine accumulated in >53-mm aggregates but not in smaller particles. The enrichment of SOM in fungal-derived glucosamine suggests that the accrual of hyphal cell-wall residues is an important process in the three NT agroecosystems which leads to higher SOM storage in surface soil concurrent with an increase in aggregate stability. The other soils, having a lower clay plus silt content, exhibited no significant differences in POM-C, MWD, and total amino sugars between NT and CT management systems. We suggest that at lower clay plus silt contents the beneficial potential for NT to sequester microbial-derived SOM is lower because of limited physical stabilization.

Abbreviations: CT, conventional tillage • d.w., dry weight • MWD, mean weight diameter • NT, no-tillage • POM-C, particulate organic matter carbon • SOM, soil organic matter • TOC, total organic carbon


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
Materials and methods
 Results
 Discussion
 Conclusions
 REFERENCES
 
SOIL ORGANIC MATTER is composed of a wide range of above and belowground plant (primary resources) and microbial (secondary resources) residues at all stages of decay with various decomposition rates which result from complex interactions among biological, chemical, and physical processes in soil (Swift et al., 1979). Besides mineralization, the primary and secondary resources are subject to microbial resynthesis (e.g., polysaccharides), direct transformation (e.g., lignin), and selective preservation (e.g., lignin and some microbial cell-wall constituents) (Kögel-Knabner, 1993; Zech and Kögel-Knabner, 1994). Hence, the composition and activity of the microbial biomass is an important determinant in the amount and quality (defined as structural composition) of SOM that accumulate in soils (Elliott and Coleman, 1988).

Agricultural management practices have been shown to influence strongly the size and composition of the microbial community in soil (Beare et al., 1992; Frey et al., 1999). Beare (1997) showed that litter placement exerts a pronounced influence on the composition of decomposer communities. Conventional tillage (CT) systems, where litter is buried, favor a bacterial-dominated community, whereas in the surface litter and soil environment of no-tillage (NT) systems, filamentous fungi are relatively more abundant. This shift in community structure has important implications for SOM storage. According to Beare et al. (1992), the larger microbial biomass and greater contribution of a dominantly bacterivorous fauna found on buried litter is consistent with greater litter C losses and presumably lower C assimilation in CT than NT agroecosystems. The promoted active growth of fungal hyphae in NT agroecosystems can result in the enmeshment of soil particles and formation of aggregates (Gupta and Germida, 1988; Tisdall et al., 1997). Elliott and Coleman (1988) suggested that hyphae are important in the formation and stabilization of macroaggregates when soils are converted from CT to NT management, resulting in the accrual of SOM.

In recent years, the response of sensitive SOM pools to different agricultural management practices has been studied in some detail with respect to degradation with cultivation (e.g., Elliott, 1986; Cambardella and Elliott, 1992; 1994; Beare et al., 1994a,b) and to accretion after conversion to grassland (Jastrow, 1996; Jastrow et al., 1996). In many models (e.g., Parton et al., 1987), such SOM pools correspond more or less to the active and intermediate pool. Much experimental work (e.g., Cambardella and Elliott, 1992; Beare et al., 1994a,b; Wander et al., 1994; Franzluebbers and Arshad, 1997) has examined land-use and management effects on the particulate organic matter (POM) fraction, which can be characterized as partly decomposed plant debris (Golchin et al., 1994). In contrast, efforts to investigate the response of microbial residues to changes in land use and management are scarce (Cambardella and Elliott, 1994; Elliott et al., 1996).

Bacterial and fungal biomass can be estimated by direct counts of bacterial cells and fungal hyphae (Frey et al., 1999). However, no direct method exists to quantify the necromass. In the past, glucosamine (Hicks and Newell, 1983; Zelles et al., 1990) and muramic acid (Millar and Casida, 1970; Moriarty, 1983) have been used as indicators of fungal and bacterial biomass, respectively. Chitin, a polymer of N-acetyl glucosamine, is a common constituent of fungal cell walls and yields only glucosamine upon hydrolysis. N-acetyl muramic acid is exclusively found in the peptidoglycan of the prokaryotic cell wall, where it alternates with N-acetyl glucosamine at a ratio of 1:1 (Brock and Madigan, 1988). More recently, Durska and Kaszubiak (1983), West et al. (1987), and Jörgensen et al. (1995) proposed that glucosamine and muramic acid do not characterize the biomass of fungi and bacteria but rather their residues. Chantigny et al. (1997) suggested that the glucosamine and muramic acid contents in soil is a measure of total (living and decomposing) microbial cell-wall mass.

The objective of this study was to assess the relative contribution of bacterial and fungal necromass to SOM in long-term CT and NT agroecosystems to verify the hypothesis that higher SOM concentrations in NT management, as compared with CT management, are partly due to stable or stabilized components of the microbial necromass, in particular fungal necromass. Our approach was to use the amount of total amino sugars in soil as a comparative estimate for microbial contributions to SOM (Benzing-Purdie, 1984; Stevenson, 1994) under six long-term CT and NT agroecosystems in North America. The proportion of fungal and bacterial cell-wall residues was assessed from the glucosamine and muramic acid pattern and compared with fungal and bacterial biomass. In two soil pairs, we additionally investigated the amino sugar pattern in aggregate fractions to relate microbial-derived SOM to aggregation.


   Materials and methods
TOP
 ABSTRACT
 INTRODUCTION
 Materials and methods
Results
 Discussion
 Conclusions
 REFERENCES
 
Site and Soil Characteristics and Sample Preparation
Site and soil characteristics and a detailed description of sampling and processing methods used in this study have been presented in Frey et al. (1999). Briefly, intact soil cores were collected from CT and NT plots at six long-term field experiments in May and June, 1996 (Table 1) . Four sites (Mandan, ND; Sidney, NE; Stratton, CO; Bushland, TX) are located in the Great Plains. The other two sites represent soils developed under tallgrass prairie (Manhattan, KS) and bluegrass sod (Lexington, KY). Samples from three field replicates for each tillage treatment were collected by depth increment (0–5 and 5–20 cm) at each site, except for Stratton, CO, where only two replicates were included in the experimental design. Also at Stratton, conventional tillage was not included as a treatment in the experimental plots; therefore, samples were collected from an adjacent farmer's field that had been under continuous CT cultivation for at least 50 yr. Additional information regarding management history, current management practices, and soil characteristics at these sites can be found in the references listed in Table 1.


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  		Table 1 Site characteristics (adopted from Frey et al., 1999)

 
The study of Frey et al. (1999) showed that fungal and bacterial abundance and biomass are affected by management in the 0- to 5-cm increment only. Therefore, we used only this increment to investigate fungal and bacterial residues in these soils. Six 5.6-cm-diam. soil cores were collected from each treatment replicate and composited. All samples were gently broken apart, passed through an 8-mm sieve, and air dried. Crop residues, root fragments and rocks larger than 2 mm were removed before analysis. Texture and particulate organic matter carbon (POM-C) were determined according to the method described by Cambardella and Elliott (1992). The size distribution of water-stable aggregates was measured according to the method described by Cambardella and Elliott (1993). Briefly, a 100-g subsample of air-dried soil was wet sieved through a series of three sieves to obtain the following aggregate size fractions: 2000 to 8000 mm, 250 to 2000 mm, 53 to 250 mm, and <53 mm. Soil remaining on each sieve was backwashed into an aluminum pan, dried overnight at 50°C, and weighed. In each aggregate-size class, the sand content was determined to calculate sand-corrected contents of total organic carbon (TOC), total nitrogen (Nt), and amino sugars (Elliott et al., 1991). The amount of soil in each aggregate size class was used to calculate the mean weight diameter (MWD) for each treatment replicate (Kemper and Rosenau, 1986).

Chemical Analyses
Total carbon (Ct) and total nitrogen (Nt) were determined by dry combustion on a C–N–H–S analyzer (Elementar GmbH, Hanau, Germany). Since the soil samples were free of CaCO3, Ct was assumed to represent TOC.

Amino sugar analysis was carried out according to Zhang and Amelung (1996). Briefly, soil samples (containing about 0.3 mg N) added with 50 mg myo-inositol (internal standard) were hydrolyzed for 8 h with 6 M HCl (10 mL) in a N2 atmosphere. Impurities in the acidic hydrolysates were removed by neutralization with 0.4 M KOH solution. Aldononitrile derivatives of amino sugars were prepared by dissolving the samples in 0.3 mL derivatization reagent [32 mg hydroxylamine hydrochloride mL-1 and 40 mg 4-(dimethylamino)pyridine mL-1 in pyridine-methanol (4:1 v/v)] and heating at 75–80°C for 30 min. After acetylation with 1 mL acetic anhydride at 75 to 80°C for 20 min, dichlormethane was added, and excess derivatization reagents were removed with four washing steps of 1 M HCl and distilled water (1 mL each). The final organic phase was dried with dry air at 45°C and finally dissolved in 0.3 mL ethyl acetate-hexane (1:1 v/v). Separation and quantification of amino sugars was carried out by gas liquid chromatography on a HP 5870 gas chromatograph (Hewlett-Packard, Palo Alto, CA) equipped with a flame ionization detector and a 30 m by 0.2-mm ID (0.33 µm) fused silica column (HP Ultra-2), and using methylglucamine as a recovery standard.

Note on Terminology and Possible Sources of Error
For interpretation of the data, we assumed that muramic acid exclusively represented bacterial cell-wall mass, whereas glucosamine represented fungal cell-wall mass, bacterial cell-wall mass, and some contribution of exoskeleton from microarthropods. According to Chantigny et al. (1997), we corrected the glucosamine concentrations for the bacterial glucosamine by assuming that muramic acid is not present in fungal cell walls and that the ratio of glucosamine to muramic acid in the peptidoglycan of the bacterial cell wall is 1:1 (Brock and Madigan, 1988). Additional minor sources of bacterial glucosamine are teichoic acids and lipopolysaccharides in the cell walls of gram-positive and gram-negative bacteria, respectively (Parsons, 1981). But because of very low contents of the non-peptidoglycan glucosamine in bacteria, we assumed the glucosamine concentrations reported in this paper representing fungal glucosamine plus an unknown contribution of glucosamine from microarthropods.

Unfortunately, the contribution of microarthropods to the glucosamine content at the different sites could not be accounted for. According to literature data, however, the proportion of microarthropods to total microbial and faunal biomass is much smaller than that of fungi. Lauenroth and Milchunas (1991) examined the invertebrate community composition for the Pawnee National Grassland in northeastern Colorado. After conversion to dry weight, the total biomass of microarthropods was calculated as 0.20 g m-2 (0- to 60-cm soil depth) compared with 38.0 g fungal biomass m-2 (0- to 30-cm soil depth). At Horseshoe Bend, Georgia, Beare (1997) compiled data on the biomass of microbial and faunal groups for different agroecosystems. In summer–autumn samples, the average biomass of microarthropods was 0.17 g C m-2 under NT and 0.06 g C m-2 under CT. About half of those amounts were found in winter–spring samples. In contrast, the fungal biomass was 79.9 (NT) and 74.0 (CT) g C m-2 for the summer–autumn samples and 71.1 (NT) and 69.0 (CT) g C m-2 for the winter–spring samples (Beare, 1997). The percentage of total biomass never exceeded 0.1 for microarthropods, whereas fungal biomass always accounted for more than 30% of the total biomass. Considering similar turnover rates of microarthropods and fungi and a comparable fraction of dead organisms entering the refractory substrate pool (Hunt et al., 1987), i.e., chitin as a major constituent of microarthropod exoskeletons and fungal cell walls, the contribution of microarthropods to the soil glucosamine pool is two orders of magnitude lower than that of fungi for Horseshoe Bend.

Even if variation in the biomass of microarthropods resulting from differences in climate and soils is considered, differences in the contribution of microarthropods to the soil glucosamine pool would always be within the analytical error of the amino sugar method. For the sake of simplicity, we therefore use the term "fungal glucosamine" when referring to glucosamine not derived from bacteria.


   Results
TOP
 ABSTRACT
 INTRODUCTION
 Materials and methods
 Results
Discussion
 Conclusions
 REFERENCES
 
Microbial Biomass in Soils under Conventional Tillage and No-Tillage
In all soils, microbial biomass was dominated by bacteria, except for the NT plots at Lexington, KY (Table 2) . No-tillage agroecosystems consistently had larger fungal biomass, as compared with CT agroecosystems, whereas bacterial biomass was significantly larger in NT relative to CT at Sidney, NE, and Manhattan, KS, only. At Mandan, ND, and Stratton, CO, bacterial biomass was smaller in NT than in CT systems, outbalancing the higher fungal biomass. At all sites except Manhattan, the ratio of fungal biomass to bacterial biomass was significantly larger in soils under NT management, as compared with CT soils. We concurrently observed significantly larger values for TOC, POM-C, and MWD (Table 3) with larger fungal biomass in NT soils at Sidney, Manhattan, and Lexington. At Mandan, Stratton, and Bushland, TOC, POM-C, and MWD did not concur with the larger fungal biomass in the NT systems. Bacterial and fungal biomass in surface soil under NT and CT appeared to be independent of texture (Frey et al., 1999).


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  		Table 2 Bacterial and fungal biomass{dagger} in the soils under conventional (CT) and no-tillage (NT) cropping systems; n = 3, numbers in parentheses represent standard errors (from Frey et al., 1998). Please note that in contrast to the original paper, biomass data were not converted to biomass C assuming a C content of fungi and bacteria of 40%, but shown directly

 

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  		Table 3 Some physical and chemical characteristics of the soils under conventional (CT) and no-tillage (NT) cropping systems; n = 3, numbers in parentheses represent standard errors (from Frey et al., 1999)

 
Amino Sugar in Soils under Conventional Tillage and No-Tillage
Total amino sugar contents varied between 1120 and 3393 mg kg-1 soil (Table 4) , and corresponded well with previous reports on amino sugar contents in other North American soils under agriculture (Benzing-Purdie, 1984; Zhang et al., 1997). Glucosamine was by far the dominant compound, while mannosamine and muramic acid were minor constituents. At Sidney, Manhattan, and Lexington, the content of all amino sugars was larger under NT than under CT. The difference was more pronounced for glucosamine than for muramic acid, which resulted in higher ratios of glucosamine to muramic acid under NT than under CT (Fig. 1) . In addition, the glucosamine content was higher in NT than under CT at Stratton. At the other sites, no significant changes in the amino sugar pattern occurred as a result of the different management systems.


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  		Table 4 Amino sugar concentrations in the soils under conventional (CT) and no-tillage (NT) cropping systems; n = 3, numbers in parentheses represent standard errors

 


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  		Fig. 1 Ratios of glucosamine to muramic acid for the conventional ({square}) and no-tillage soils ({blacksquare}) at Mandan, ND, Stratton, CO, Bushland, TX, Sidney, NE, Manhattan, KS, and Lexington, KY. Mean values with standard errors are shown, n = 3. Pairs of bars with the same letter signify no sigificant difference at P < 0.05 between the two cropping systems

 
The comparison between microbial biomass estimates and the total amino sugar contents revealed that there was a relationship between both sets of parameters (Fig. 2) . The functional analysis according to Webster (1989) gave a slope and an intercept . But the relationship was not strong . That is, the Bushland and Stratton soils had comparable amino sugar contents, although they differed in their microbial biomass by a factor of more than three.



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  		Fig. 2 Scatter plot of the microbial biomass versus the amino sugar content in conventional ({circ}) and no-tillage (•) soils at Mandan, ND, Stratton, CO, Bushland, TX, Sidney, NE, Manhattan, KS, and Lexington, KY. Mean values with standard errors are shown, n = 3. The solid line represents the functional relation between both sets of parameter with its slope and its intercept

 
There was no consistent trend between the ratio of fungal to bacterial biomass and the ratio of fungal-derived glucosamine to bacterial-derived muramic acid (not shown). While the ratio of fungal biomass to bacterial biomass was significantly higher in NT than in CT at all sites, the ratio of glucosamine to muramic acid in NT soils exceeded that in CT soils at Sidney, Manhattan, and Lexington only.

To assess possible effects of the different management systems on the source and quality of SOM, concentrations of single SOM constituents are given on a TOC basis. The total amino sugar concentrations varied between 106 and 139 g kg-1 TOC (Fig. 3a) . At all sites, SOM tended to be enriched in microbial-derived amino sugars in NT soils as compared with CT soils; however, these differences were significant for Sidney, Manhattan, and Lexington only. The concentrations of glucosamine ranged from 64 to 85 g kg-1 TOC. Because glucosamine is the dominant amino sugar, its concentration generally mirrored the total amino sugar pattern (Fig. 3b). However, differences in the glucosamine concentrations between NT and CT systems were always larger than differences in the total amino sugars. In addition to Sidney, Manhattan, and Lexington, Stratton also showed a significantly higher glucosamine concentration in the NT agroecosystem.



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  		Fig. 3 Concentration of SOM present as total amino sugars (A) and glucosamine (B) as related to the TOC content in conventional ({square}) and no-tillage soils ({blacksquare}) at Mandan, ND, Stratton, CO, Bushland, TX, Sidney, NE, Manhattan, KS, and Lexington, KY. Mean values with standard errors are shown, n = 3. Pairs of bars with the same letter signify no sigificant difference at P < 0.05 between the two cropping systems

 
Amino Sugars within Aggregate Size Classes
At Sidney, Manhattan, and Lexington, higher contents of glucosamine and muramic acid in NT soils coincided with a larger MWD, whereas at the other sites, no effects of the different management systems were observed for the two parameters.

To examine the concentration and distribution of fungal and bacterial cell-wall residues within aggregates, we investigated four different aggregate-size classes of the Sidney and Lexington soils. The distribution of soil mass across the aggregates showed a shift to larger aggregate fractions under NT management (Table 5) . Total organic carbon concentrations, expressed on whole aggregate basis, increased with increasing aggregate-size class at Sidney. On a sand-free basis, TOC increased significantly with increasing aggregate size at Sidney, whereas this increase was not observed at Lexington. Six et al. (1999) observed the same trends at both sites. They suggested that the similar TOC across aggregate size classes is related to the specific mineralogy of the Lexington soil. At both Sidney and Lexington, the higher TOC content in whole soil under NT, compared with CT, was due to both a shift towards larger aggregates and higher TOC concentrations within the aggregate-size classes.


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  		Table 5 Distribution of soil mass across aggregate size fractions and the content of total organic carbon (TOC) and total nitrogen (Nt) in the size separates of the Lexington, KY, and Sidney, NE, soils under conventional (CT) and no-tillage (NT) cropping systems; n = 3, numbers in parentheses represent standard errors

 
The amino sugar contents within different size fractions followed a pattern similar to TOC (Table 6) . In all size classes, more amino sugars were found in NT agroecosystems than in CT agroecosystems, irrespective of how expressed, whole aggregate basis or sand-free basis. However, in the Sidney soil the higher sand content in aggregate-size fractions under CT, as compared with NT, reduced differences between CT and NT when data were expressed on a silt plus clay basis. In CT soils, the ratios of glucosamine to muramic acid were almost constant across the size classes (Fig. 4) . In NT soils, the ratios of glucosamine to muramic acid exceeded those in CT soils in all size classes, except for the <53-µm fraction. The Sidney soil under NT management showed a continuous increase in amino sugars and in the ratio of glucosamine to muramic acid with increasing aggregate size. At Lexington, the amino sugar contents and the ratio of glucosamine to muramic acid peaked in the 53- to 250-µm and 250- to 2000-µm classes.


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  		Table 6 Amino sugar concentrations in the Lexington, KY, and Sidney, NE, soils under conventional (CT) and no-tillage (NT) cropping systems; n = 3, numbers in parentheses represent standard errors

 


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  		Fig. 4 Ratios of glucosamine to muramic acid for the aggregate-size classes <53 µm ({square}), 53 to 250 mm (), 250 to 2000 mm (), and 2000 yo 8000 mm ({blacksquare}) of the conventional (CT) and no-tillage soils (NT) at Sidney, NE and Lexington, KY. Mean values with standard errors are shown, n = 3. Pairs of bars with the same letter signify no sigificant difference at P < 0.05 between the aggregate-size classes. Values of the NT treatment with * are significantly different than corresponding values of the CT plots at P < 0.05

 
Under CT management, the contribution of SOM present as total amino sugars and as glucosamine, respectively, was similar in all size separates at Sidney, whereas at Lexington it was lower in the two macroaggregate fractions than in the smaller size classes (Fig. 5) . In NT agroecosystems, SOM in the three larger aggregate fractions was enriched in amino sugars as compared with SOM of the respective aggregate size classes in soil under CT. Differences were more pronounced for glucosamine.



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  		Fig. 5 Concentration of SOM present as total amino sugars (A) and glucosamine (B) as related to the TOC content in the aggregate-size classes <53 µm ({square}), 53 to 250 mm (), 250 to 2000 mm (), and 2000 to 8000 mm ({blacksquare}) of the conventional (CT) and no-tillage soils (NT) at Sidney, NE and Lexington, KY. Mean values with standard errors are shown, n = 3. Pairs of bars with the same letter signify no sigificant difference at P < 0.05 between the aggregate-size classes. Values of the NT treatment with * are significantly different than corresponding values of the CT plots at P < 0.05

 

   Discussion
TOP
 ABSTRACT
 INTRODUCTION
 Materials and methods
 Results
 Discussion
Conclusions
 REFERENCES
 
Amino Sugar Contents versus Microbial Biomass
Muramic acid concentrations in living bacterial biomass are larger for gram-positive bacteria than for gram-negative bacteria. Millar and Casida (1979) measured a muramic acid content of 3.4 ± 0.5 g kg-1 (d.w.) for seven species of gram-negative bacteria, 9.6 ± 1.9 g kg-1 (d.w.) for five species of gram-positive bacteria, and 37.6 ± 3.5 g kg-1 (d.w.) for spores of three species. Similar concentrations were reported by Durska and Kaszubiak (1983) and Jörgensen et al. (1995). Since gram-positive bacteria by far dominate in soil (Millar and Casida, 1970), we assumed a concentration of 10 g muramic acid kg-1 soil bacteria (d.w.) as a reasonable concentration. It has been shown that fungi have a glucosamine concentration that varies between 26 and 260 g kg-1 (d.w.) (Blumenthal and Roseman, 1957; Chen and Johnson, 1983); we assumed a mean concentration of 150 g kg-1 soil fungi (d.w.).

On the basis of the above assumptions and on the contents of bacterial and fungal biomass in the soils (Table 2), we estimated the muramic acid and glucosamine contents present in the soil biomass. The total concentrations of muramic acid and glucosamine in soil were higher than the estimated concentrations present in soil biomass by factors of 26 to 82 and 54 to 745, respectively (Table 7) , suggesting a much longer turnover time of these cell-wall constituents in soil than that of the living microorganisms. The large variation across soils and between soil management systems indicates that muramic acid and glucosamine are not suitable as indicators for bacterial and fungal biomass, since no constant conversion factor could be delineated. In spite of the uncertainties in the estimation of muramic acid and glucosamine present in soil microorganisms, the pronounced enrichment of both substances in soil, as compared with microbial biomass, suggests that bacterial-derived muramic acid and, in particular, fungal-derived glucosamine must be stable and/or stabilized in the soil environment. The estimation also suggests that bacterial cell walls are more susceptible to decomposition than fungal cell walls. Nakas and Klein (1979) followed the decomposition of 14C-labeled microbial cell components in a semi-arid grassland soil in Colorado and found that bacterial cell walls were usually degraded to a greater extent than fungal cell walls.


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  		Table 7 Enrichment factors of muramic acid and glucosamine found in 1 g of soil as compared with muramic acid and glucosamine present in bacteria and fungi in 1 g of soil. Muramic acid concentrations in living bacteria were estimated on the basis of a muramic acid content of 10 g kg-1 soil bacteria (d.w.), and living soil fungi were assumed to contain 150 g glucosamine kg-1 (d.w.). Values in parentheses represent worst-case estimates based on lowest and highest muramic acid concentrations found in bacteria [2.6 and 19.0 g kg-1 (d.w.)] and lowest and highest glucosamine concentrations found in fungi [26 and 260 g kg-1 (d.w.)] as reported by Blumenthal and Roseman (1953), Millar and Casida (1970), Chen and Johnson (1983), Durska and Kaszubiak (1983), and Jörgensen et al. (1995)

 
Although all sites were sampled at the same phenological time of the year, we cannot exclude effects of different meteorological conditions to soil fungal and bacterial biomass, because soil microorganisms respond very rapidly to soil moisture changes (Schnürer et al., 1986; Chantigny et al., 1996). Frey et al. (1999) found a significant positive relationship between soil moisture content and bacterial and fungal biomass, with a stronger relationship for fungi. Because of drought in early 1996, the Bushland soil had a low soil moisture content which may have resulted in a distinctively low microbial biomass (Frey et al., 1999). In contrast to soil biomass, which shows a considerable fluctuation in the course of a year (Chantigny et al., 1996) and can be used as an early indicator for changing soil management (Powlson et al., 1987; Frey et al., 1999), it may be possible to use the amino sugar pattern as a measure for longer-term changes within a soil ecosystem.

Amino Sugar Pattern in Conventional Tillage and No-Tillage Soils
All parameters differentiated NT plots from CT plots at Sidney, Manhattan, and Lexington, whereas at Mandan, Stratton, and Bushland only the relative proportion of soil fungi and bacteria responded to different management systems. As outlined by Frey et al. (1999), NT systems favor fungal growth at all sites. However, the fungal-derived amino sugar concentrations did not, or only insignificantly, follow this response of fungi to NT at Mandan, Stratton, and Bushland. This may be partly due to the different land-use histories and the shorter duration of the NT management systems at these sites (Frey et al., 1999). Sidney had been under virgin prairie sod and Lexington under bluegrass sod for at least 50 yr prior to arable use. In contrast, Mandan, Stratton, and Bushland were established on land that had been under conventional wheat-fallow cultivation for 30 to 50 yr prior to experiment initiation. Hence, SOM levels were depleted at the latter sites at the start of the experiments, and treatment effects would require accumulation of SOM constituents in addition to a reduction in further SOM losses (Frey et al., 1999). Since Mandan, Stratton, and Bushland were established only 12 to 15 yr prior to our sampling, as opposed to 22 to 26 yr for the other sites, the build-up and the decomposition of amino sugars may not have reached equilibrium yet. However, the different histories of the field experiments cannot fully account for this observation.

When assessing the behavior of amino sugars in CT and NT agroecosystems, one has to consider the clay and silt content. Hassink (1997) showed a close positive relationship between the proportion of primary particles <20 µm in soil and the amounts of C and N that were associated with this fraction in the top 10 cm, and that fine-textured soils have higher organic C and N contents than coarse-textured soils when supplied with similar input of organic material. A principal factor responsible for this observation is the ability of SOM to associate with clay and silt particles (Martin and Haider, 1986). A greater portion of the newly formed microbial products becomes and remains physically protected with increasing clay content (van Veen et al., 1985). Amino sugars are highly enriched in the clay-sized separates (Zhang et al., 1998), and Zhang et al. (1997) showed a significant positive relationship between the clay plus silt contents and the amino sugars accumulated in a range of cultivated prairie soils. Following the conclusions of Hassink (1996, 1997), we suggest that soils with a higher clay plus silt content may show a larger saturation deficit (the difference between the actual and the maximum amount of C associated with the <20-µm fraction) when under cultivation. Hence, with establishment of NT there is a more pronounced decrease in the saturation deficit possible at Sidney, Manhattan, and Lexington as compared with the other sites that have lower clay plus silt contents. The beneficial effects of clay and silt may also explain why at Sidney differences between CT and NT management system are the largest. In this soil, there is a large difference in the clay plus silt content between CT and NT (64 vs. 85%). Differences between CT and NT for POM-C and total amino sugars may be the result of tillage, but it is strongly accentuated by the textural difference. This is exemplified by the amino sugar pattern across aggregate-size classes. While on a whole aggregate basis, the amino sugar concentrations in the larger aggregate-size classes of soil under NT exceeded those in soil under CT two-threefold, on a sand-free basis differences were much smaller, albeit still significant.

Clay also indirectly affects SOM accrual in NT agroecosystems. Franzluebbers and Arshad (1996, 1997) showed a strong positive relationship of the clay content with macroaggregation and POM-C. Particulate organic matter both forms and is incorporated into macroaggregates (Six et al., 1998). Hence, at the sites with a higher clay content (under NT management at Sidney, Manhattan, and Lexington), there is a higher capacity for macroaggregate formation and accumulation of POM within macroaggregates in the absence of tillage disturbance. Since microorganisms preferentially feed on easily utilizable carbon sources (such as plant-derived carbohydrates), a higher POM content leads to higher microbial activity and release of microbial residues (Angers and Giroux, 1996) like amino sugars, resulting in higher aggregation and greater physical protection of the microbial residues.

Amino Sugar Pattern and Soil Aggregation
Fungal biomass has often been related to soil aggregate stability (Gupta and Germida, 1988; Drury et al., 1991). This observation is due to the strategy of fungi to explore new substrates. Fungal hyphae are actively growing towards and into small microhabitats and decompose the available SOM (Coleman and Crossley, 1996). As a result, extracellular polysaccharides are released and fungal hyphae entangle soil particles, which are considered to be key processes in the formation of macroaggregates (Tisdall and Oades, 1982; Haynes and Francis, 1993; Six et al., 1998). In that sense, formation of macroaggregates is a function of available OM; i.e., fresh plant residues (as previously discussed).

In our study, MWD increased concurrently with the fungal biomass in the NT systems at Sidney, Manhattan, and Lexington. At the other sites, the increase in fungal biomass was not associated with an increase in MWD. In contrast, glucosamine as well as muramic acid had the same response to soil management as MWD. Chantigny et al. (1997) emphasized the discrepancy in the literature concerning the relationship between microbial biomass and MWD. They argued that microbial biomass is subject to fluctuations due to environmental conditions that do not necessarily affect soil aggregation and followed the proposal of Angers (1992) that more stable organic compounds must be responsible for stabilization of aggregates.

The amino sugar measurements showed that the CT soils at Sidney and Lexington had almost constant values for the concentrations of amino sugars present in SOM and for the ratios of glucosamine to muramic acid across the four aggregate-size classes. The additional amino sugars stored in NT soils were distributed into the three larger size classes, whereas the amino sugars in the <53-mm fraction remained unaffected by the management systems. The higher ratio of glucosamine to muramic acid in the three larger fractions confirms the association of large microaggregates and macroaggregates with hyphal cell-wall residues and is consistent with the observation that fungal activity exerts a pronounced influence on the formation of aggregates. In a laboratory incubation experiment, Guggenberger et al. (1999) showed that soil biota, in particular, soil fungi led to rapid formation of macroaggregates. During later phases of the experiment, fungal and bacterial biomass declined rapidly; however, macroaggregates remained stable. This suggests that more recalcitrant compounds like cell-wall residues were involved in the aggregate stabilization. The amino sugar data showed that at Mandan, Stratton, and Bushland there was no enrichment of such stable microbial residues, providing further evidence that the amino sugar pattern may be a good measure to investigate the impact of soil microorganisms on aggregation (Chantigny et al., 1997). However, a clear cause and effect relationship between aggregation and accumulation of cell-wall residues still needs to be evaluated; possibly there is a positive feedback between both factors.

This study shows that NT agroecosystems lead not only to an enrichment of chemically labile microbial compounds like carbohydrates within macroaggregates (Hu et al., 1995), but also to compounds of a higher intrinsic resistance to microbial attack; i.e., cell-wall constituents represented by amino sugars. Additional protection of these primarily fungal cell-wall residues may occur by formation of organomineral complexes with clay- and silt-sized separates and by inclusion within aggregates.


   Conclusions
TOP
 ABSTRACT
 INTRODUCTION
 Materials and methods
 Results
 Discussion
 Conclusions
REFERENCES
 
The amino sugar pattern in soil provided a useful approach to follow the incorporation of fungal and bacterial cell-wall residues into SOM. At long-term experiments at Sidney, Manhattan, and Lexington, establishment of NT agroecosystem resulted in increasing concentrations of total amino sugars and in particular of glucosamine. Higher concentrations of SOM present as total amino sugars and as glucosamine characterize a shift in SOM quality. The enrichment of SOM in fungal-derived glucosamine suggests that the accrual of hyphal cell-wall residues is an important process in NT agroecosystems leading to a higher SOM storage in the surface soil as compared with the surface soil of CT agroecosystems.

The accrual of hyphal cell-wall residues under NT took place concurrently with an increase in MWD, and the additional fungal-derived compounds were accumulated in macro- and large microaggregates. No clear cause–effect relationships can be drawn at this point, but the study provides evidence of a complex interaction of accumulation of fungal and bacterial cell-wall residues with fungal and bacterial biomass, POM storage, and aggregation. For the NT soils at Sidney, Manhattan, and Lexington, we hypothesize a positive feedback mechanism between the stabilization of aggregates by hyphal cell-wall residues and the physical protection of cell-wall residues inside aggregates from microbial decomposition. Such cell-wall residues may represent a microbial-derived intermediate SOM pool that is accumulated in NT agroecosystems as proposed by Elliott et al. (1996). The high N content stored in stabilized microbial cell-wall residues may also partly explain the improved N retention observed in many NT agroecosystems (Paul et al., 1997). Compared with more labile organic substances like simple polysaccharides, microbial cell-wall biopolymers show a higher intrinsic chemical stability. Their degradation after loss of physical protection by destruction of aggregates may thus not be as rapid.Black Tanaka 1991


   ACKNOWLEDGMENTS
 
We greatly appreciate the support and assistance provided by participating scientists at each field site: Robert Blevins and Edmund Perfect at Lexington, KY; Ardell Halvorson at Mandan, ND; Ordie R. Jones at Bushland, TX; Drew Lyon at Sidney, NE; Gary Peterson at Stratton, CO; and Charles Rice at Manhattan, KS. In particular, we acknowledge the thought, time, and resources these scientists have invested in the development and maintenance of the long-term tillage comparison experiments at their respective sites. Without these experiments, examination of long-term tillage effects on soil properties would not be possible. Collection of soil samples was made possible by a United States Department of Agriculture grant (COL-9503436) to E.T. Elliott, K. Paustian, and S.D. Frey. G. Guggenberger gratefully acknowledges a grant from the German Academic Exchange Service (DAAD) for a post-doctoral scholarship at the Natural Resource Ecology Laboratory.

Received for publication February 5, 1998.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 Materials and methods
 Results
 Discussion
 Conclusions
 REFERENCES
 




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