Environ. Sci. Technol. 2005, 39, 5442-5448
Role of Wheat-Residue-Derived Char in the Biodegradation of Benzonitrile in Soil: Nutritional Stimulation versus Adsorptive Inhibition P I N G Z H A N G , † G U A N G Y A O S H E N G , * ,† YUCHENG FENG,‡ AND DAVID M. MILLER† Department of Crop, Soil, and Environmental Sciences, University of Arkansas, Fayetteville, Arkansas 72701, and Department of Agronomy and Soils, Auburn University, Auburn, Alabama 36849
Previous studies demonstrated that crop-residue-derived chars are effective adsorbents for pesticides and substantially reduce their biodegradation in soils. In contrast, the nutrients in the chars may stimulate cell growth and hence enhance the biodegradation. This work investigated the role of a wheat-residue-derived char in the nutritional stimulation and adsorptive inhibition of biodegradation of benzonitrile in a soil. The biodegradation was measured at 78 mg/L of benzonitrile, an initial concentration much higher than the half-saturation constant of the degrading organism (∼18 mg/L). The degradation was much faster in the extract of char-amended soil (CAS) than in those of soil and washed-char-amended soil (WCAS). The degradation was also faster in CAS slurry than in slurries of soil and WCAS until ∼88% of benzonitrile degraded in char-containing slurries, where the aqueous-phase concentration was ∼0.25 mg/L. Cell density was higher in extracts and slurries in the presence of the char nutrients than in the absence of them. Analysis of nutrient elements in extracts, along with measuring degradation in soil extract with nutrient supplements and subsequent stepwise multiple-regression, suggested that the char nutrients stimulated cell growth and degradation of benzonitrile, for which P was primarily responsible. Further degradation of benzonitrile beyond 88% in the presence of char was slow, suggestive of the adsorptive inhibition. The biodegradation of benzonitrile in CAS thus occurred through a fast-to-slow process, the former step being due primarily to the stimulation by soluble P of char and the latter phase to the adsorptive inhibition.
Introduction Biodegradation of organic contaminants and pesticides in soils is influenced by characteristics of degrading microorganisms as well as contaminant physicochemical properties (e.g., solubility) and processes (e.g., sorption) (1). Biodegradation may be slow because microbial activity and growth may be limited by the supply of nutrients (2). Many nutrients are often at less-than-optimal concentrations for microbial * Corresponding author phone: (479) (479) 575-3975; e-mail:
[email protected]. † University of Arkansas. ‡ Auburn University. 5442
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ENVIRONMENTAL SCIENCE & TECHNOLOGY / VOL. 39, NO. 14, 2005
growth and metabolism (3). Supplementary nutrients usually stimulate biodegradation (4, 5) and shorten adaptation periods prior to degradation, particularly if substrate C is abundant (6-8). In other cases, nutrients do not have significant influence (6) or may even decrease the biodegradation of certain organic contaminants (2, 9). Sorption usually reduces biodegradation by decreasing aqueous-phase contaminant concentrations. While sorbed contaminants may be partially accessed by microorganisms in certain systems (10-13), aqueous-phase contaminants are the most bioaccessible and desorption is often a prerequisite for the biodegradation of sorbed contaminants (13-17). Biodegradation of pesticides in agricultural soils may be complicated by the widespread presence of chars. Wood chars produced ex situ are increasingly applied into agricultural soils as supplements of inorganic elements and liming substitutes (18-20). Soil chars are also widely generated in situ by field burning of vegetation, a common postharvest agricultural practice for disposal of crop residues, weed control, and immediate land clearing and land-use change. Crop-residue-derived chars are known to contain many inorganic nutrients. We reported that a wheat-residuederived char had a composition of 14.3% carbon, 0.64% nitrogen, 1.46% phosphorus, 21.0% potassium, 3.36% calcium, 0.89% magnesium, 0.63% sulfur, and other nutrient elements (sodium, iron, manganese, zinc, copper, boron, and aluminum) (21). When in their bioavailable (soluble) forms in soil solution, some of these elements may significantly influence microbial activity and hence biodegradation. Chars are also known as highly effective adsorbents for pesticides. Hilton and Yuen (22) reported that sorption of substituted ureas and s-triazines by several Hawaiian soils that previously received burning of sugar cane trash remained high after oxidative removal of soil organic matter by hydrogen peroxide and was substantially reduced on ignition (with the intention of removing char). It was speculated that the sorption was a property of both easily oxidized soil organic matter and peroxide-resistant soil chars resulting from cane trash burning. We found that sorption of diuron by the wheatresidue-derived char described above was 400-2500 times higher than that by a soil with 2.1% organic matter (23). The sorption by the soil in the presence of the char increased with increasing char content within the tested range of 0-1% (by weight). Aging of the char in the soil for up to 12 months did not substantially reduce its adsorptivity for diuron, indicating its refractory surface properties (21). Similarly, effective adsorption of benzonitrile by the char resulted in a 10-fold increase in sorptivity of the soil amended with 1% of the char. As a result of the enhanced sorption that dramatically reduced the aqueous-phase benzonitrile concentration, biodegradation of benzonitrile at a total initial concentration of 1.06 mg/L in the 1% char-amended soil was substantially reduced (24). The reported initial aqueousphase equilibrium benzonitrile concentration prior to biodegradation was 3.7 × 10-2 mg/L. Due to the lack of the measured half-saturation constant of the degrading organism employed, the low initial aqueous-phase concentration of benzonitrile was presumed to be limiting on the biodegradation. The influence of char nutrients on biodegradation of pesticides in soils remains to be understood. It can be hypothesized that char may stimulate biodegradation by supplying nutrients that may otherwise be limiting in soils containing high concentrations of pesticides. In contrast, adsorption to char may effectively reduce the aqueous-phase pesticide concentrations and subsequently become limiting 10.1021/es0480670 CCC: $30.25
2005 American Chemical Society Published on Web 06/09/2005
on the degradation. The present study was conducted to measure the biodegradation of benzonitrile at a high initial concentration in a soil in the presence of a wheat-residuederived char. The objective was to evaluate the role of char in providing nutrients that may stimulate biodegradation and in pesticide adsorption that may inhibit biodegradation in soil. Understanding these processes will help delineate the influence of crop-residue-derived chars on the environmental fate of pesticides in agricultural soils.
Experimental Section Solids and Media. A silt loam soil and a wheat-residuederived char from our previous studies were used. Details on their collection, preparation, and characteristics were described by Yang and Sheng (21). The soil was collected from an agricultural field in Stuttgart, Arkansas. The soil had a mechanical composition of 17.1% sand, 60.4% silt, and 22.5% clay with 2.1% organic matter. Without records of crop residue burns, the soil was presumed to have minimal chars. The soil was air-dried, ground, and passed through a 1-mm sieve. The char was collected by burning air-dried wheat (Triticum aestivum L.) residue on a 1 × 1 m stainless steel plate in an open field under natural conditions. A previous study showed that the char was a highly effective adsorbent for benzonitrile (24). To remove char nutrients, the char was suspended in 0.1 M HCl solution and shaken overnight; the supernatant was removed after centrifugation. This procedure was repeated once in the same fresh acid solution and then twice in 0.01 M HCl solution. The pH of the char was then adjusted to 10.2 with 0.1 M NaOH solution. Residual Cl- and Na+ were removed by thorough washing of the char with deionized water six times. The char with a final pH of 9.3 was dried in an oven at 50 °C. Two char-amended soil samples were prepared by mixing 99 g of the soil with 1 g of the original char or a predetermined quantity (3 times the Ks (data shown later) as well as a low initial cell density in this study, the growing conditions were achieved that allowed one to observe the stimulatory role of char nutrients. As effective sorption affected degradation, however, the Monod kinetics was not attempted to analyze the degradation data. Degradation in Extracts. The biodegradation of benzonitrile in the extracts of soil, CAS, and WCAS, all containing 78 mg/L of benzonitrile, is shown in Figure 1, in which the degradation is expressed as percent benzonitrile degraded. Benzonitrile in soil extract was slowly degraded with
