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a Dep. of Horticulture, Oregon State Univ., 4017 ALS, Corvallis, OR 97456
b School of Natural Resources and Dep. of Geological Sciences, The Ohio State Univ., 2021 Coffey Rd., Columbus, OH 43210
c Dep. of Plant Pathology, The Ohio State Univ., 1680 Madison Ave., Wooster, OH 44691
Corresponding author (stonea{at}bcc.orst.edu)
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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1 yr. Suppression was sustained by the degradation of the less decomposed coarse and mid-sized POM fractions. After these fractions stabilized in mass, suppression was lost. Plant constituents were highly degraded during composting before amendment to sand. Compost-derived POM composition changed little as suppression was supported for 1 yr. In contrast, aromatic and aliphatic contents and alkyl- and O-alkyl C declined as suppression was lost. Suppressive POM was similar in composition to forest soil organic horizons and soil unprotected light fraction (ULF), suggesting that the least-decomposed soil physical fractions may be the only fractions compositionally capable of supporting suppression of DO in field soils.
Abbreviations: CPMAS, cross-polarization magic angle spinning • DM, dry matter • DO, damping-off • DR-FTIR or DRIFT, diffuse reflectance Fourier transform infrared • LF, light fraction • NMR, nuclear magnetic resonance • OM, organic matter • PLF, protected light fraction • POM, particulate organic matter • SOM, soil organic matter • ULF, unprotected light fraction
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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During the past two decades, major advances have been made in the understanding and predictive commercial use of OM-mediated suppression of root rots in container mixes. Producers of nursery stock discovered that potting mixes prepared with composted manures or tree barks suppressed root rots caused by Pythium and Phytophthora spp., while severe losses occurred in dark, decomposed sphagnum peat mixes (Hoitink et al., 1997). They also observed that the quality of the organic material in some manner affected the longevity of the suppressive effects. It has been shown that composted hardwood barks, composted pine barks, and light peat support suppression of root rot for 2 yr, 9 mo, and several weeks, respectively, while dark peats do not support suppression for any length of time (Boehm et al., 1993; Hoitink et al., 1997). Longevity of suppression was related to the proportion of bacterial biological control agents supported by a specific type of OM: 25% of the culturable bacterial species in highly suppressive composted hardwood barks have some ability to suppress Pythium root rot, compared with 10% in moderately suppressive light peat and <1% in nonsuppressive dark peat (Boehm et al., 1993, 1997).
To our knowledge, only one attempt has been made to directly relate OM composition or active C fractions such as particulate organic matter (POM) with disease suppression. Boehm et al. (1997) used 13C cross-polarization magic angle spinning nuclear magnetic resonance (13C CPMAS NMR) spectroscopy to analyze the composition of suppressive light peat in a potting mix as it decomposed and lost suppressiveness. The carbohydrate content, mostly present as cellulose, declined as suppressiveness was lost. Bacterial species composition changed to that characteristic of a highly mineralized soil fraction, populations of biocontrol agents declined, and Pythium populations increased, leading to the conclusion that the carbohydrate content and bioavailability of the peat regulated biocontrol of Pythium root rot.
The objective of this work was to characterize the mass and composition of compost-derived POM in sand as it decomposed and the system lost suppressiveness to Pythium damping-off (DO), a type of root rot. Spectroscopic techniques (diffuse reflectance Fourier transform infrared [DR-FTIR] and 13C CPMAS NMR) were used to analyze the composition of sawdust-bedded dairy manure-derived POM as it decomposed in sand over a 506-d period. The composition of suppressive and conducive POM was then related to literature values for agricultural and forest soil POM fractions.
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MATERIALS AND METHODS |
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A peat–sand mix, referred to hereafter as the peat mix, was prepared by blending peat into the silica sand (1:4, v/v). Dolomitic limestone [CaMg(CO3)2], gypsum (CaSO4 · 2H2O), triple super phosphate [Ca(H2PO4)2], and potassium nitrate (KNO3) were added to adjust the pH of the mixture to 6.5 and nutrient levels to a level adequate for cucumber growth as determined by soil test.
Substrate Incubation and Sampling
The peat and compost mixes were incubated in a greenhouse at 20 to 30°C in 4-L, 210-cm-tall plastic pots. Each treatment was replicated 10 times (10 pots). The temperature of the mix ranged from 18 to 23°C. Pots were watered as necessary.
Pythium Damping-Off Bioassay
Pythium ultimum inoculum was prepared using Ko and Hora's chopped potato soil medium (Ko and Hora, 1971). A mixture of moist silt loam soil (500 mL) and finely chopped potatoes (50 g) was autoclaved for 1 h on each of 2 consecutive days and inoculated with discs of P. ultimum grown on potato dextrose agar. The inoculated mixture was incubated at room temperature for 1 wk and then air-dried, ground with a mortar and pestle, and sieved to a 1- to 2-mm particle size. A 2-L composite sample of each mix (compost mix and peat mix) was placed in a plastic bag and inoculated with P. ultimum (0.5 g L-1 mix). Bags were gently rotated to incorporate inoculum into the mix while minimizing abrasion of compost and peat particles. A pure sand treatment was also tested. Mixes were then evenly distributed into five 400-mL Styrofoam cups. Eight cucumber seeds (Straight Eight) were planted 1 cm deep in each cup. Pots were incubated for 10 d at 20°C, 16-h illumination (225 µE m2 s-1) and fertilized every other day (30 mg L-1 Peter's Professional 20-20-20, Scott's Sierra Horticultural Products, Marysville, OH). Disease severity was rated 10 d after planting according to the following rating scale: 1 = symptomless; 2 = emerged but wilted or with visible lesions on the hypocotyl; 3 = post-emergence damping-off; and 4 = pre-emergence damping-off. A mean disease severity rating (n = 8) was determined for each pot (5 pots per treatment).
Particulate Organic Matter Analyses
The compost mix was sampled at 83, 293, 391, and 506 d after potting, composited, frozen in liquid N, and stored at -20°C until analyzed. Particulate organic matter (POM) was decanted with water from four 150-g samples from each treatment and wet-sieved to recover the 53-µm to 2-mm particle size class. Four additional samples were decanted and fractionated into three size fractions: 53 to 420 µm (fine), 420 µm to 1 mm (midsize), and 1 to 2 mm (coarse). Decantation with water was used to remove POM from the sand fraction because (i) it is less likely to alter the composition of the POM than density fractionation methods (Magid et al., 1996), and (ii) POM was easily separated from sand using this method. All fractions were oven-dried overnight at 110°C and weighed to determine POM content.
Determination of Particulate Organic Matter Composition
Particulate organic matter composition was determined by DR-FTIR and 13C-CPMAS NMR spectroscopic methods. All spectroscopic measurements were made on dried POM fractions from the compost mix.
Diffuse Reflectance Fourier Transform Infrared Spectroscopy
Particulate organic matter samples were ground with a synthetic sapphire mortar and pestle. Subsamples (3 mg) were reground with 297 mg of previously ground KCl and stored in a vacuum dessicator over P2O5 for 48 h. This mixture was packed tightly in a small sample cup and smoothed with the edge of a glass slide. The surface was then roughened with the tip of a needle to minimize specular reflectance. Samples were analyzed with a Mattson Cirus FTIR (Mattson Equipment, Madison, WI) equipped with a Harrick Preying Mantis diffuse reflectance cell (Harrick Scientific, Ossining, NY). All spectra were obtained by averaging 100 scans at 2 cm-1 resolution from 4000 to 500 cm-1. Analyses of spectral data were performed with Grams/386 spectral software (Galactic Industries, Salem, NH). Spectral interpretation was conducted on two regions of interest: aliphatics (3015–2805 cm-1) and the lower wavenumbers (1825–865 cm-1). There are few peaks of interest in organic matter spectra at other wavenumbers (Stevenson, 1982). Vibrational peaks were assigned to functional groups and organic matter constituents as described in Table 1.
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Rationale for the Use of Subtraction Spectra
Most DR-FTIR spectral analyses of composting organic matter have used peak ratios to monitor changes in chemistry (Inbar et al., 1989, 1991). Peak ratios such as 1385/2930 (COO-,CH3/aliphatic CH) increase as composting progresses (Inbar et al., 1989). Inbar et al. (1989) concluded through the use of such ratios that polysaccharide content declines and aromatic content increases during the composting process. However, it is difficult to quantify changes in organic matter chemistry using this approach due to peak overlaps and the preponderance of poorly defined baselines. Tseng et al. (1996) instead used second derivatives, curve fitting, and peak area integration to more quantitatively analyze changes in chemistry of organic matter during the composting process. To use curve fitting, the number of peaks in the region of interest and the shape of the bands must be known, and the baseline must be well-defined (Pierce et al., 1990). In the spectral region from 1835 to 950 cm-1, compost generates many overlapping bands of unknown quantity and shape, so curve fitting in this region may generate inaccurate estimates of constituent concentration. In addition, the baseline in the lower wavenumbers is essentially undefined. Therefore, we did not attempt to quantify changes in constituent concentration, but used baseline correction, spectral averaging, and spectral subtraction to assess qualitative, yet absolute, changes in peak intensities over time.
Samples were packed reproducibly to minimize spectral variability. Baselines were corrected to a mean absorbance value at 865 cm-1 to minimize variability due to baseline drift. Spectral replicates were averaged to generate a spectrum most representative of sample chemistry. Average spectra were then subtracted to generate spectra representing only peaks changing in intensity between compost harvest dates. Assuming that baseline-corrected spectra all possess similar undefined baselines in the lower wavenumbers, spectral subtraction should eliminate the need to identify the baseline. However, specific conditions must be met for spectral subtraction to be valid. Subtraction must be applied to absorbance spectra with absorbance values no greater than 0.7 absorbance units so that Beer's law is obeyed (Griffiths and de Haseth, 1986), and subtraction spectra should not contain derivative-like peaks (P. R. Griffiths, Univ. of ID, personal communication, 1995). These conditions were met in this study.
Carbon-13 Cross-Polarization Magic Angle Spinning Nuclear Magnetic Resonance Spectroscopy
Nuclear magnetic resonance (13C CPMAS NMR) spectra of POM were produced on a Bruker MSL-300 NMR spectrometer (Bruker Instruments, Fremont, CA) operating at 75.4 MHZ by C. E. Cottrell at the Ohio State University Chemical Instrument Center. The data were acquired with a spinning rate of 4500 rps, a contact time of 1 ms and an acquisition time of 0.034 s with a 4-s repetition rate. Interferograms were transformed by an exponential match apodization filter with 100-Hz line-broadening, Fourier-transformed, and deconvolved with WinNMR (Bruker Instruments) spectral software. Spectra were divided into the regions 200 to 160 ppm (carbonyl/carboxyl-C), 160 to 110 ppm (aromatic-C), 110 to 45 ppm (O-alkyl-C), and 45 to 10 ppm (alkyl-C) as in Golchin et al. (1994). The total signal intensity and the proportion of the total intensity contributed by each type of C were determined by integration with Grams/386 spectral software.
Experimental Design and Statistical Analyses
The substrate incubation and all cucumber bioassays were conducted according to a completely randomized design. All one-way analysis of variance (ANOVA) tests were performed with Sigma Stat software (SPSS Science, Chicago, IL). Separation of means was based on Fisher's least significant difference (LSD, P = 0.05).
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RESULTS |
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DISCUSSION |
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Temporal Changes in Particulate Organic Matter Size Fractions
The foregoing observations suggest that suppression was sustained by the degradation of the coarse and midsized POM fractions. The decomposition of these fractions generated the more decomposed fine fraction, as the mass of the fine fraction declined only after the losses in the coarse and midsized fractions had ceased (Fig. 1). Both coarse and midsized fractions contained greater aromatic and carbohydrate peak intensities than the fine fraction (Fig. 5). The less decomposed midsized and coarse particles dominated total POM as suppression was sustained, while the more decomposed fine fraction dominated as suppression was lost (Fig. 1).
The early degradation of the larger-sized fractions is typical during POM/light fraction (LF) decomposition (Aita et al., 1997). In a study of the short-term kinetics of 14C-labeled straw residues applied to soil, LF-C in the >2000-µm fraction had a half-life of 53 d. Physical fractionation of the larger-sized fractions generated the smaller-sized fractions; when the >2000-µm fraction stabilized, the intermediate-sized fractions ceased to increase in mass. The quantity of labeled C in the fine fraction increased during the first 34 d and then remained constant (Aita et al., 1997). These dynamics are similar to those observed in this study.
Compost and Particulate Organic Matter Composition
The freshly separated sawdust-bedded dairy manure spectra (Fig. 3) appeared similar to spectra of the wood used as bedding (data not shown) and included several high-intensity peaks in the carbohydrate region (990–1160 cm-1). The prominent peaks in the more decomposed POM spectra at the end of composting and the beginning of decomposition in sand are also present in "lignin" spectra generated from plant tissue after alkaline hydrolysis: 1030, 1128, 1160, 1221, 1270, 1328, 1370, 1420, 1460, 1509, 1595, and 1650 cm-1 (Fidalgo et al., 1993; Fig. 3). However, these peaks are much broader in the well-decomposed POM than the sharp peaks observed in the fresh plant tissue spectra, presumably due to degradation and alteration of lignin (P. R. Griffiths, Univ. of ID, personal communication, 1995). Some studies have reported or assumed that lignin is highly recalcitrant and not decomposed during composting (Lynch and Wood, 1985; Inbar et al., 1989), but others have reported significant reductions (up to 70%) in lignin content and composition (Horwath and Elliott, 1996). By the time the compost was mixed with sand at the beginning of this experiment, plant constituents were already highly degraded and chemically altered, resulting in a complex, poorly defined organic matrix. Nevertheless, the POM spectra (Fig. 3) appeared more similar in terms of peak composition to spectra of hydrolyzed plant tissue than to spectra of humic substances (hydrolyzed tissue and humic spectra not shown) (Stevenson, 1982; Fidalgo et al., 1993).
Changes in DR-FTIR peak intensities were very dramatic during composting but of much smaller magnitude during subsequent decomposition of POM in sand (Fig. 2a). Aliphatic (3015–2805 cm-1), carbohydrate (1160, 1060 cm-1), and aromatic (1595, 1509 cm-1) peaks declined in intensity as total POM decomposed over the 506-d period (Fig. 2a and b). Interestingly, the changes in peak intensity of greatest magnitude occurred not during the year while suppression was supported, but in the 3 mo thereafter as suppression was lost (Fig. 2b, Fig. 4).
Comparison with Wood-Decomposition Studies
The dramatic decline in total POM over the first 300 d of decomposition in the compost mix (Fig. 1), concomitant with virtually invariant composition as determined by DR-FTIR and NMR spectroscopy (Fig. 2b, Fig. 4; Table 3), was similar to trends observed in wood-decomposition studies. Three major stages in natural wood decomposition over very long (e.g., 15–50 yr) periods have been documented through the use of 13C NMR spectroscopy (Preston et al., 1990; Baldock and Preston, 1995). In the first stage, carbohydrate levels increase. In the second stage, carbohydrates decline, and aromatic and carbonyl C increase due to the recalcitrant nature of lignin and the increased oxidation of organic molecules during degradation. In the third stage, little change in chemistry occurs. Losses of mass (density) with little change in chemistry have also been reported for birch and beech wood decomposition by white-rot fungi (Martinez et al., 1991; Hortling et al., 1992). In the present study, the composted sawdust-bedded dairy manure underwent similar changes in composition to those observed during natural wood decomposition. During the composting process, carbohydrates were degraded more rapidly than lignin (Table 3), similar to wood stage 2. While suppression was supported, the organic matter was relatively nonselectively degraded, similar to wood stage 3 (Table 3) (although degradation of aliphatics was detected by DR-FTIR; Fig. 2b). However, unlike the trends in these long-term wood degradation studies, this material underwent a fourth stage after Day 391, in which POM composition shifted fairly dramatically as determined by both DR-FTIR and NMR (Fig. 2b, Fig. 4; Table 3).
Change in Particulate Organic Matter Composition as Suppression Was Lost
We have no obvious explanation for the sudden change in composition between Days 391 and 506. The DR-FTIR data suggest that the microbial community shifted to a selective degradation of aromatics/aliphatics or, in other words, ceased degrading carbohydrates. However, the 13C CPMAS NMR data indicate that degradation of O-alkyl C occurred during the period when suppression was lost (Table 3). O-alkyl C is typically considered to be carbohydrate C but can also include non-carbohydrate structures such as ether-C in saturated 5- or 6-membered rings, amino acid C, or aliphatic C with OH groups (Schnitzer, 1990). The apparent decline in putative carbohydrate content (as suggested by the NMR spectra) would agree with a decline in carbohydrate content (also detected by 13C CPMAS NMR) observed during the loss of suppression of Pythium DO in a peat-based potting mix (Boehm et al., 1997). However, a reduction in the proportion of alkyl-C was also observed as suppression was lost in this sawdust-bedded dairy manure compost-derived POM (Table 3), while only the O-alkyl-C content declined during the loss of suppression in the peat system (Boehm et al., 1997). Therefore, a different hypothesis might be that the O-alkyl C detected by NMR after suppression was lost might be OH-substituted alkyl-C, in agreement with the FTIR-detected reduction in aliphatic peak intensities.
Problems Associated with Spectroscopic Analyses
It is not surprising that DR-FTIR and 13C CPMAS NMR spectroscopic data do not completely agree. Both methods may generate somewhat erroneous compositional data when applied to a complex material such as decomposing organic matter. In DR-FTIR spectra there is considerable peak overlap (Table 1), and in highly decomposed plant tissues it is difficult to make accurate peak assignments. Nuclear magnetic resonance data may also generate biased estimates of composition due to variation in cross-polarization rates for different carbon types, spinning sidebands generated by low magic angle spinning rates, peak overlap, and multiple peak assignments (Cook et al., 1996). However, a better method for the nondestructive characterization of decomposing organic matter currently does not exist.
While the DR-FTIR and 13C CPMAS NMR data do not completely agree, some general conclusions can be made. During the period when suppression was supported, the mass of coarse and midsized POM declined while total POM composition changed little. Later, as suppression was lost, a greater change in composition was detected while very little change in mass occurred. Therefore, regardless of the spectroscopic technique employed, suppression appears to be sustained by the relatively nonselective degradation of the larger-particle-sized, least decomposed POM.
Degradation of Aliphatics
Reductions in aliphatics content were observed throughout composting and decomposition in sand as determined by DR-FTIR spectroscopy. In contrast, no change in the proportion of aliphatics was detected by 13C CPMAS NMR spectroscopy between Days 81 and 391, while a slight decline was detected thereafter (Table 3). Carbon-13 CPMAS NMR spectroscopy has been used to elucidate decomposition processes in a variety of organic materials as described previously. In all materials studied, O-alkyl C content declined and alkyl-C content increased in proportion, while changes in carbonyl and aromatic C contents were variable (Baldock et al., 1992). The increase in alkyl C has been hypothesized to be due to microbially synthesized or transformed alkyl-C (Kögel-Knabner et al., 1992a, 1992b) or the selective preservation of polymethylene C in plant tissues (Hatcher et al., 1983). Microbial synthesis of alkyl-C after glucose addition was reported by Baldock et al. (1989)( 1990a, 1990b) and during the decomposition of peat (Harvey et al., 1989) and lignin (Ellwardt et al., 1981). The structure of these recalcitrant alkyl structures is not known (Kögel-Knabner et al., 1992a, 1992b). Interestingly, certain peaks in the DR-FTIR aliphatics region appear to represent more labile, plant-derived aliphatics (e.g., 2890 cm-1), which decomposed primarily during composting, while others represent more recalcitrant aliphatics (e.g., 2965, 2934, 2920, 2850 cm-1), which decomposed throughout composting and decomposition in sand (Fig. 4b). Unfortunately, this region is poorly characterized (Table 1), and to our knowledge no previous studies have attempted to relate these chemically distinct peaks in DR-FTIR spectra to SOM constituents such as microbially synthesized or plant-derived aliphatics.
In studies of wood decomposition, very little change in alkyl-C was detected by 13C CPMAS NMR relative to increases observed in other types of organic matter (Baldock and Preston, 1995). This may be due to three possible factors: the relatively low alkyl-C content of fresh wood, little microbial production of alkyl-C during wood decomposition, and little transformation of mobile alkyl-C into rigid alkyl-C by cross-linking or association with soil mineral particles (Baldock and Preston, 1995). These findings lend support to the lack of increase in aliphatics content observed during the decomposition of the sawdust-bedded dairy manure compost. However, no previous studies have reported either an absolute or proportionate decline in alkyl-C as decomposition progressed, which was clearly observed in both the DR-FTIR (Fig. 2b) and NMR (Table 3) spectra in this work.
Diffuse reflectance Fourier transform infrared spectroscopic methods detected selective degradation of aliphatics as suppression was both supported and lost, while NMR spectroscopic methods detected degradation of alkyl-C as suppression was lost. These findings indicate that these constituents may be an important substrate for the microbial community involved in suppression of Pythium DO. Because aliphatic substrates found in OM relatively late in decomposition are considered to be microbially recalcitrant, this is an interesting finding and should be investigated further.
Comparison of Peat, Compost, and Soil Particulate Organic Matter Decomposition
In the work of Boehm et al. (1997), suppression appeared to be supported by the degradation of carbohydrates alone, whereas in the present study, suppression in compost-amended sand appeared to be supported by the relatively nonselective degradation of coarse, slightly decomposed POM. This difference in OM degradation is probably due to the difference in substrate: carbohydrates are typically selectively metabolized during relatively short-term peat decomposition (Hammond et al., 1985). In contrast, wood may be nonselectively degraded (Martinez et al., 1991; Hortling et al., 1992).
The composition of compost-derived POM observed in this work as determined by 13C CPMAS NMR was similar to that of unprotected POM/LF from a variety of soils and forest litter and organic horizons (Table 3). Compost-derived POM sampled on Days 83, 391, and 506 compost-derived POM were closest in composition to the free LF and forest litter, although if the relatively low alkyl-C content was disregarded and decomposition level was determined on the basis of O-alkyl-C content, they were also close in composition to Of and Oh horizons (forest soil organic horizons). As noted previously, decomposed wood contains a lower proportion of alkyl-C than other types of organic materials (Baldock and Preston, 1995), so alkyl-C is not a region useful for comparing the decomposition levels of wood-derived OM with OM derived from other plant tissues. The O-alkyl content of the compost-derived POM is in the unprotected light fraction (ULF) range and higher than that of the occluded LF, indicating that the compost-derived POM sampled on Days 83 to 391 was relatively lightly decomposed. Interestingly, between 391 and 506 d, as the material became more highly decomposed and suppression was lost, the O-alkyl content of the compost-derived POM dropped below the ULF, closer to the level of protected light fraction (PLF), which is generally more decomposed than ULF.
Soil organic matter physical fractions have been shown to undergo fairly consistent patterns and rates of decomposition regardless of residue composition or soil type (Hassink, 1995). Therefore, differences in overall SOM turnover rates in different soil types are due to differences in the distribution of OM into pools of varying turnover rates, and not to differences in the turnover rates of pools among soil types (Hassink, 1995). Unprotected light fraction composition has been shown to be highly independent of soil type, environment, and residue type, while PLF composition is more variable (Golchin et al., 1994). Therefore, POM-driven ecological processes may be more related to residue loading rates and degree of protection of POM than to POM origin or initial composition. The independence of unprotected POM composition and dynamics suggests that the relationships between compost-derived POM and suppression of Pythium DO observed here might also be observed in field systems.
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ACKNOWLEDGMENTS |
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Received for publication September 6, 1999.
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REFERENCES |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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