Published online 1 May 2008
Published in J Environ Qual 37:848-857 (2008)
DOI: 10.2134/jeq2007.0448
© 2008 American Society of Agronomy, Crop Science Society of America, and Soil Science Society of America
677 S. Segoe Rd., Madison, WI 53711 USA
TECHNICAL REPORTS
Organic Compounds in the Environment
Atrazine Dissipation in s-Triazine–Adapted and Nonadapted Soil from Colorado and Mississippi: Implications of Enhanced Degradation on Atrazine Fate and Transport Parameters
L. Jason Krutza,*,
Dale L. Shanerb,
Cesare Accinellic,
Robert M. Zablotowicza and
W. Brien Henryd
a USDA-ARS, Southern Weed Science Research Unit, P.O. Box 350, Stoneville, MS 38776
b USDA-ARS, Water Management Research Unit, 2150 Centre Ave., Fort Collins, CO 80526
c Dep. of Agro-Environmental Science and Technology, Univ. of Bologna, V. le Fanin 44, Bologna, Italy 40127
d USDA-ARS, Corn Plant Host Resistance Unit, Dorman 117 Box 9555, Mississippi State, MS 39762
* Corresponding author (jason.krutz{at}ars.usda.gov).
Received for publication August 22, 2007.
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ABSTRACT
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Soil bacteria have developed novel metabolic abilities resulting in enhanced atrazine degradation. Consequently, there is a need to evaluate the effects of enhanced degradation on parameters used to model atrazine fate and transport. The objectives of this study were (i) to screen Colorado (CO) and Mississippi (MS) atrazine-adapted and non-adapted soil for genes that code for enzymes able to rapidly catabolize atrazine and (ii) to compare atrazine persistence, Q10, β, and metabolite profiles between adapted and non-adapted soils. The atzABC and/or trzN genes were detected only in adapted soil. Atrazine's average half-life in adapted soil was 10-fold lower than that of the non-adapted soil and 18-fold lower than the USEPA estimate of 3 to 4 mo. Q10 was greater in adapted soil. No difference in β was observed between soils. The accumulation and persistence of mono-N-dealkylated metabolites was lower in adapted soil; conversely, under suboptimal moisture levels in CO adapted soil, hydroxyatrazine concentrations exceeded 30% of the parent compounds' initial mass. Results indicate that (i) enhanced atrazine degradation and atzABC and/or trzN genes are likely widespread across the Western and Southern corn-growing regions of the USA; (ii) persistence of atrazine and its mono-N-dealkylated metabolites is significantly reduced in adapted soil; (iii) hydroxyatrazine can be a major degradation product in adapted soil; and (iv) fate, transport, and risk assessment models that assume historic atrazine degradation pathways and persistence estimates will likely overpredict the compounds' transport potential in adapted soil.
Abbreviations: DEA, desethylatrazine • DIA, deisopropylatrazine • FC, field capacity • HA, hydroxyatrazine • HPLC, high-performance liquid chromatography • LOQ, limit of quantitation, PCR, polymerase chain reaction
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INTRODUCTION
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ATRAZINE [6-chloro-N2–ethyl-N4-isopropyl-1,3,5-triazine-2,4-diamine] is a soil-applied s-triazine herbicide that provides residual weed control in corn (Zea mays L.), sorghum (Sorghum bicolor L.), sugarcane (Saccharum officinarum L.), and turf. In regional surface and ground water monitoring studies, atrazine is often detected more frequently and at higher concentrations than other pesticides (Clark and Goolsby, 2000; Kolpin et al., 1996; Kolpin et al., 2000; Lerch et al., 1998; Pereira and Hostettler, 1993; Scribner et al., 2000; Zablotowicz et al., 2006b). Higher atrazine concentrations and detection frequencies in surface and ground water are attributed to the herbicide's widespread use, mobility, and persistence in the environment (USEPA, 2006). With application rates ranging from 29 to 34 million kg yr–1, atrazine is the second most frequently applied pesticide in the USA (USEPA, 2006). Atrazine's average soil/water partitioning coefficient on most soils is less than 3 (USEPA, 2006), indicating the potential for atrazine to be mobile in the environment (Wauchope, 1978). However, recent developments may require modelers and regulatory agencies to reconsider the assumption that atrazine is only moderately susceptible to degradation in soil.
The USEPA indicates that atrazine's average half-life in soil under aerobic laboratory conditions is 3 to 4 mo (USEPA, 2006), which is consistent with Wauchope's review of the literature (Wauchope et al., 1992). Atrazine's moderate half-life in soil has been attributed to the halogen and N-alkyl substituents, which historically have impeded microbial degradation of the s-triazine ring (Wackett et al., 2002). However, in the mid-1990s, bacteria able to catabolize atrazine were isolated (Mandelbaum et al., 1995; Radosevich et al., 1995). Subsequently, the genes and enzymes responsible for atrazine catabolism by soil bacteria were identified (Fig. 1
). Homologs of these genes have been detected in atrazine-degrading bacteria from geographically distinct regions, indicating that the pathway(s) in Fig. 1 is likely widespread. If bacteria in agricultural soils have developed similar metabolic abilities, then enhanced atrazine degradation is likely.
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Fig. 1. Proposed metabolic pathway(s) responsible for the rapid dissipation of atrazine in Colorado (CO) and Mississippi (MS) atrazine-adapted soil. Abbreviations denote genes coding for the following enzymes: atzA, atrazine chlorohydrolase; trzN, s-triazine hydrolase; atzB, hydroxyatrazine ethylaminohydrolase; atzC, N-isopropylammelide isopropylaminohydrolase; TrzD, cyanuric acid amidohydrolase; atzD, cyanuric acid hydrolase; atzE, biuret hydrolase; atzF, allophanate hydrolase; and trzF, allophanate hydrolase (Boundy-Mills et al., 1997; Cheng et al., 2005; de Souza et al., 1998; Fruchey et al., 2003; Martinez et al., 2001; Mulbry et al., 2002; Sadowsky et al., 1998; Seffernick et al., 2002; Shapir et al., 2002; Shapir et al., 2005; Shapir et al., 2006; Smith et al., 2005; Topp, 2001; Wackett et al., 2002).
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Enhanced degradation is the phenomenon whereby a soil-applied pesticide is rapidly degraded by a population of microorganisms that has developed the ability to use the pesticide as a carbon, energy, and/or nutrient source because of previous exposure to the pesticide or an analog. Enhanced atrazine degradation has been demonstrated in agricultural soils from Argentina, Belgium, Canada, France, and the USA (Barriuso and Houot, 1996; Hang et al., 2003; Houot et al., 2000; Ostrofsky et al., 1997; Pussemier et al., 1997; Shaner et al., 2007; Shaner and Henry, 2007; Vanderheyden et al., 1997; Yassir et al., 1999; Zablotowicz et al., 2006b).
Common fate and transport models, including RZWQM, PRZM3, and Opus2, contain submodels that describe pesticide degradation as a function of temperature and moisture (Ma et al., 2000; Ma et al., 2004). A generalized form of the first-order kinetics model commonly used by fate and transport models to describe pesticide degradation as a function of soil temperature and moisture has been described by Beulke et al. (2005):
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where C(t) is the pesticide concentration in soil at time t (mg kg–1), Co is the initial pesticide concentration (mg kg–1), k(T,
) is the rate constant under actual temperature T (°C) and soil moisture , k is the first-order rate constant in reciprocal days (d–1), T1/2 is the time required for Co to reach one half its original value (d), kref is the degradation rate constant in reciprocal days (d–1) at reference temperature and moisture, Q10 is the factor by which degradation increases when T increases by 10°C, T is the actual temperature (°C), Tref is reference temperature, is actual soil moisture (% field capacity [FC]), ref is reference soil moisture (40% FC), and β is the moisture exponent.
Sensitivity analysis conducted on RZWQM, Opus2, GLEAMS, and PRZM2 indicates that pesticide persistence is a sensitive input parameter (Bakhsh et al., 2004; Chinkuyu et al., 2005; Ma et al., 2004; Muller et al., 2003; Neurath et al., 2007). Consequently, if atrazine persistence is drastically reduced in adapted soils, then models that continue to rely on historic rates of atrazine degradation cannot accurately predict its fate and transport in adapted soils.
The objectives of this study were (i) to screen Colorado (CO) and Mississippi (MS) adapted and non-adapted soil for the atzA, atzB, and atzC genes (i.e., atzABC); (ii) to compare atrazine dissipation and mineralization kinetics among CO and MS adapted and non-adapted soil as a function of soil temperature (10 and 20°C) and moisture (40 and 70% FC); (iii) to compare Q10 and β between adapted and non-adapted soil; and (iv) to compare desethylatrazine (DEA), deisopropylatrazine (DIA), and hydroxyatrazine (HA) concentrations as a function of temperature, moisture, and time between adapted and non-adapted soil.
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Materials and Methods
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Site History and Soil Collection
s-Triazine Adapted and Nonadapted Soil from Colorado
Classification of atrazine adapted and non-adapted soil was based on the method of Shaner et al. (2007). Adapted soil was collected from the 0- to 10-cm depth on 12 July 2006 from a field that had been under dry land corn production since 2002. The field had been treated with atrazine since 2002 and was treated with atrazine on 12 June 2006 at 1.1 kg ha–1. Non-s-triazine–adapted soil was collected from the 0- to 10-cm depth on 13 July 2006 from a grass waterway that had not received an atrazine application for at least 5 yr. Samples of adapted and non-adapted soil were passed through a 2-mm sieve and stored at 5°C until study initiation. The soil texture, organic matter content, and water holding capacity of these soils are reported in Table 1
.
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Table 1. Soil texture, organic matter content (OM), and water-holding capacity (–33 kPa) of atrazine-adapted and nonadapted soils from Colorado and Mississippi.
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s-Triazine Adapted and Nonadapted Soil from Mississippi
The site history for the s-triazine–adapted soil from MS has been previously described (Krutz et al., 2007; Zablotowicz et al., 2007). Briefly, the field had been under reduced tillage, planted to corn, and treated with atrazine since 2000. In 2006, the field was planted to corn and treated with atrazine on 15 Mar. 2006 at a rate of 2.2 kg ha–1, and soil from the 0- to 10-cm depth was collected on 20 Apr. 2006. Non-adapted soil was collected on 20 Apr. 2006 from a field with no prior atrazine exposure history from a depth of 0- to 10-cm. Adapted and non-adapted soils were passed through a 2-mm sieve and stored at 5°C until study initiation. The soil texture, organic matter content, and water holding capacity of these soils are reported in Table 1.
Gene Probing
DNA was isolated from CO and MS adapted and non-adapted soil using PowerSoil DNA Isolation Kits (MoBio Laboratories Inc., Carlsbad, CA). For each soil, six extractions of 250 mg of soil were performed according to the manufacturer's protocol. The DNA extracts for each soil were combined and concentrated using a Savant micro-fuge evaporator to a final volume of 300 µL, and the extract was further purified using a Wizard DNA mini-column clean-up kit (Promega, Madison, WI).
The presence of atzABC genes was determined by traditional polymerase chain reaction (PCR) using a PCR mixture containing 5 µL of DNA template, 2.5 µM of each primer, 20 µL of a 2.5x Master Mix (Eppendorf AG, Hamburg, Germany), and molecular biology–grade water to the final volume of 50 µL. Primers designed by Shapir et al. (2000) for amplification of atzA (forward: 5'CCATGTGAACCAGATCCT3'; reverse: 5'TGAAGCGTCCACAT TACC3'), atzb (forward: 5'CATGGCGGCGGCA-GGTGTG3'; reverse: 5'CCC GGGCCAGCTCCATT TCA3'), and atzC (forward: 5'AGTCAGCGAAGGGCG TAGGTATCA3'; reverse: 5'GACAAATCCGGG-AGACACAAGGTT3') genes was performed using a 5-min denaturation step at 98°C followed by 30 cycles, each consisting of a 1-min denaturation step at 95°C, a 1-min annealing step at 55°C, and a 1-min elongation step at 72°C, with a final step of extension at 72°C for 7 min. Polymerase chain reaction products were separated on a 2% agarose gel and stained with SYBR Green I (Sigma-Aldrich Corp., St. Louis, MO) using 100 bp DNA Ladder (Sigma-Aldrich Corp.) as molecular weight standards.
Enrichment cultures were established from soil suspensions of the adapted and non-adapted soils using procedures described elsewhere (Zablotowicz et al., 2007).
Five grams of soil were suspended in 50 mL of sterile phosphate buffer (0.01 mol L–1, pH 6.8) containing 32 mg L–1 of atrazine in 250-mL screw-top Erlenmeyer flasks in triplicate and incubated at 28°C and 50 rpm on a rotary incubated shaker. Suspension aliquots (2 mL) were removed every 3 to 7 d, extracted with methanol, and analyzed by high-performance liquid chromatography (HPLC). Enrichments that demonstrated 90% atrazine degradation were transferred to 50 mL of Vogels N-free medium until the third positive enrichment was obtained. DNA was isolated from the third enrichment using an ethanol precipitation method and was screened for the presence of atzABC by PCR as described previously.
Laboratory Experiments
Atrazine Dissipation and Metabolite Formation
Atrazine dissipation and metabolite formation were evaluated in 250-mL glass screw-top flasks. Soil (100 g dry weight equivalent) weighed into the flasks was fortified with technical-grade atrazine (99% purity) (Chemservice, Lancaster, PA) dissolved in HPLC-grade acetonitrile, resulting in an initial herbicide concentration of 1 µg g–1. Soil moisture was adjusted to 40 or 70% FC by the addition of deionized water. Flasks were sealed with Teflon-lined caps and incubated in the dark at 10 or 20 ± 2°C. At 1, 2, 4, 8, 16, 32, 45, and 60 DAT, soil (5 g) was removed from the flasks and extracted for atrazine and metabolites. The weight of each flask was measured at each extraction and water added, if needed, to maintain desired soil moisture.
Herbicide and Metabolite Extraction
Soil (5 g) was weighed into a 50-mL plastic centrifuge tube and extracted with 15 mL 80:20 (v/v) MeOH/25 mmol L–1 ammonium acetate adjusted to pH 8.0. The suspension was agitated on a horizontal shaker for 30 min and centrifuged at 8000 x g for 15 min, and the supernatant was transferred to 50-mL plastic centrifuge tubes. The extraction procedure was repeated, and supernatants were combined. The supernatant was evaporated to <5 mL at 50°C with a Rapidvap, brought to 10 mL with deionized water, and concentrated on a C18 SPE column (Thermo Electron Corp Hypersep) preconditioned with 3 mL each of methanol, ethyl acetate, methanol, and distilled water. The column was dried under negative pressure for 90 min, and atrazine, DEA, and DIA were eluted with 2 mL ethyl acetate into 2-mL volumetric tubes. Samples were fortified with an internal standard and 10 µL of 0.1 mg mL–1 of butylate dissolved in acetonitrile, brought to volume with ethyl acetate, and analyzed with gas chromatography/mass spectrometry. Subsequently, HA was eluted from the column with 2 mL 95:5 (v/v) methanol (MeOH)/0.1N HCl into 2-mL volumetric tubes. Samples were brought to volume with MeOH and analyzed by HPLC.
Gas Chromatography/Mass Spectrometry Analysis
The parent compound and N-dealkylated metabolites were quantified by monitoring the masses of atrazine (M/Z 200), DEA (M/Z 172), DIA (M/Z 173), and butylate (M/Z 146) with a gas chromatograph equipped with a MS detector (GC-17A and GC-MS QO 5050A; Shimadzu Scientific Instruments, Columbia, MD). Analyte separation was achieved on a 30-m by 0.25-mm RTZ-5 column (Restek, Bellefonte, PA) with a flow of helium at 1 mL min–1. Injection and detector temperature were held at 280°C. Initial oven temperature was held at 80°C for 1 min, ramped to 250°C at 20°C min–1, and held for 1.5 min. Total run time was 11 min. Under these conditions, the retention times of butylate, DIA, DEA, and atrazine were 6.51, 7.89, 7.96, and 8.44 min, respectively. Recovery of atrazine, DIA, and DEA from fortified soil samples was 95, 85, and 90%, respectively. Pesticide and metabolite concentrations in soil samples were adjusted based on these percent recoveries. The method limit of quantitation (LOQ) for atrazine, DIA, and DEA was 0.007 mg kg–1.
High-performance Liquid Chromatography Analysis
Hydroxyatrazine was identified and quantified by a Shimadzu 10AT HPLC separation module (Shimadzu Scientific) coupled with a Shimadzu spp. M 10A detector (Shimadzu Scientific). The HPLC was fitted with a 4.6-mm diameter by 150-mm length Alltech Econosphere C18 column. Mobile-phase solvents were HPLC grade and consisted of 63:35 (v/v) 5 mmol L–1 ammonium acetate pH 5.2/acetonitrile. The injection volume was 100 µL, and separation was achieved in the isocratic mode with a flow rate of 1 mL min–1. Under these conditions, HA was detected at 8.6 min at 236 nm. Hydroxyatrazine recovery from soil ranged from 75 to 85%, and the method LOQ was 0.007 mg kg–1.
Mineralization of 14C-ring-labeled Atrazine
Mineralization of 14C-ring–labled atrazine was evaluated in biometer flasks as previously described (Krutz et al., 2007). Briefly, samples of adapted and non-adapted soil (25 g dry weight equivalent) from CO and MS were fortified with a solution of technical-grade atrazine (99% purity) (Chemservice, Lancaster, PA) and 14C-atrazine (115 µCi/mmol specific activity, 94% radiological purity) (Sigma Chemical Company, St. Louis, MO) in deionized water. The initial herbicide concentration was 1 mg kg–1, and the initial radioactivity was 86,580 Bq kg–1. Final soil moisture contents were adjusted to 40 or 70% FC by addition of deionized water, and biometers were incubated in the dark at 10 or 20 ± 2°C. Evolved 14CO2 was trapped in NaOH and quantified by liquid scintillation spectroscopy using Hionic-Fluor (PerkinElmer, Shelton, CT). To avoid saturation by CO2, NaOH was replaced after each sampling. Soil was destructively sampled 65 d after herbicide application. Air-dried soil was manually crushed into uniform particle size, and duplicate samples (0.30 g) were weighed onto Whatman 1 Qualitative filter paper (Whatman Inc., Florham Park, NJ). Samples were combusted in a Packard model 306 oxidizer (Packard Instruments, Chicago, IL), and evolved 14CO2 was trapped in scintillation vials containing Carbo-Sorb and Permafluor (20 mL; 1+1 by volume) (Packard Elmer, Meridian, CT). Radioactivity was determined by liquid scintillation spectroscopy. The amount of 14CO2 recovered from the combusted samples was added to the cumulative 14CO2 evolved to determine the mass balance of 14C.
Statistical Analysis
The experimental design was a split-split-split-plot arranged as a randomized complete block with three replications of each treatment. Temperature was the whole plot, moisture the subplot, soils the sub-subplot, and times the sub-sub-subplot. Analysis of variance and mean separation was performed using Proc Mixed (SAS version 9.1; SAS Institute Inc., Cary, NC). All results were considered significantly different at p < 0.05. Regression analysis was used to determine the relationships between independent and dependent variables (SAS version 9.1; SAS Institute Inc.).
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Results
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Gene Probing
Whole-soil DNA analysis indicated that CO and MS non-adapted soils did not produce a positive response when amplified with specific primers for atzABC genes. Conversely, CO adapted soil amplified DNA of appropriate size range for atzABC genes. Adapted soil from MS did not amplify with primers for atzA, but appropriate size fragments were observed for the atzBC genes. Negative amplifications with atzA primers from DNA recovered directly from MS soils have been previously reported in the literature (Zablotowicz et al., 2006a). It is possible that inhibitory compounds extracted during DNA isolation from the MS soils interfered with direct PCR amplification of atzA or that gene abundance was below the limit of detection. Consequently, enrichment cultures were used to improve the ability to resolve the presence of atzA extracted during DNA isolation from whole soil.
After three-step enrichment, cultures were obtained from CO and MS adapted soils capable of at least 90% atrazine degradation within 3- to 7-d exposures. All MS and CO enrichments obtained from adapted soils positively amplified atzA, and all enrichments from MS adapted soil were positive for atzBC. Subsequent studies recovered single colony isolates from the MS enrichments that were positive for trzN (Accinelli, unpublished). Complete genetic and phenotypic characterization of MS degrading bacteria will be presented elsewhere. Conversely, of the four CO enrichments obtained from adapted soil, only two enrichments amplified atzC, and only one enrichment amplified atzB. No enrichments capable of degrading >30% of added atrazine (30 mg L–1) within a month were found from CO or MS non-adapted soils, and no positive reactions were obtained after amplification with atzABC primers.
Atrazine Dissipation and Metabolite Formation
Atrazine Dissipation
Atrazine's persistence in non-adapted soil was negatively correlated with temperature, but soils responded differently to soil moisture (Fig. 2
). Increasing the temperature 10°C decreased atrazine persistence at least 1.9-fold (Table 2
). At 10°C, increasing soil moisture had no affect on atrazine persistence. Conversely, at 20°C, increasing soil moisture reduced atrazine persistence 1.7-fold in CO soil while increasing atrazine's persistence 1.5-fold in MS soil. Yet, with the exception of the 20°C at 70% FC treatment, atrazine persistence within temperature and moisture levels was not different between non-adapted soils.
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Fig. 2. Atrazine dissipation in Colorado (CO) and Mississippi (MS) s-triazine–adapted and non-s-triazine–adapted soil as a function of incubation temperature (10 or 40°C) and soil moisture content (40 and 70% field capacity). Symbols represent the mean of three replications for each of the following treatments: 10°C at 40% field capacity (closed circles), 10°C at 70% field capacity (open circles), 20°C at 40% field capacity (closed inverted triangles), and 20°C at 70% field capacity (triangles). Lines represent the best fit of the first-order kinetics model: Ct = Coe–kt. Error bars indicate 1 SD and do not appear when smaller than the symbol for the mean.
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Table 2. Degradation rate constants (k) and half-life values for atrazine in Colorado (CO) and Mississippi (MS) atrazine-adapted (i.e., soil exhibiting enhanced atrazine degradation) and non-adapted soil as a function of temperature (10 or 20°C) and moisture (40 or 70% of field capacity).
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Atrazine persistence in CO and MS adapted soil was negatively correlated with soil temperature, but the response to moisture was different between soils. Increasing the temperature 10°C decreased atrazine persistence at least 2.8-fold. Atrazine persistence in CO soil was independent of soil moisture. Conversely, atrazine persistence in MS soil was negatively correlated with soil moisture. Within both temperature regimes, atrazine persistence was not different between CO and MS soils when incubated at 40% FC. However, at 70% FC, atrazine persistence was at least 3.7-fold lower in MS soil compared with CO soil.
Within all temperature and moisture regimes, atrazine persistence was lower in adapted than in non-adapted soil. Atrazine's half-life pooled over temperature and moisture was 13-fold lower in adapted than in non-adapted soil. These data demonstrate that atrazine persistence is drastically different between adapted and non-adapted soil. Thus, separate estimates for Q10 and β were calculated by pooling data within adapted and non-adapted soil. The best Q10 estimate for non-adapted soil was 1.9, which was derived solely from CO soils at 70% FC. Values for Q10 were not calculated for the remaining non-adapted soils because derived half-life values were extrapolated at least 47 d beyond the experimental data. The average Q10 for adapted soil obtained by pooling CO and MS soil over soil moisture was 2.9. Atrazine persistence in MS non-adapted soil and CO adapted soil was independent of soil moisture; thus, β was not calculated. In contrast, the average β values for MS adapted soil and CO non-adapted soil pooled over incubation temperature were 1.96 and 0.91, respectively.
Deisopropylatrazine
Within temperature and moisture levels, peak DIA concentrations were not different between non-adapted soils, and concentrations typically were independent of temperature, were positively correlated with moisture, and increased over time (Fig. 3
). Conversely, with the exception of 1 d after herbicide application, DIA concentrations in CO and MS adapted soil were independent of temperature, moisture, and time. Moreover, from 16 d after herbicide application until study termination, DIA concentrations never exceeded the LOQ. Consequently, peak DIA concentrations were greater in non-adapted soil than in adapted soil for the majority of the incubation, particularly under optimal soil moisture.
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Fig. 3. Deisopropylatrazine (DIA) concentrations in Colorado (CO) and Mississippi (MS) s-triazine–adapted and non-s-triazine–adapted soil as a function of incubation temperature (10 or 40°C) and soil moisture content (40 and 70% field capacity). Symbols represent the mean of three replications for each of the following treatments: 10°C at 40% field capacity (closed circles), 10°C at 70% field capacity (open circles), 20°C at 40% field capacity (closed inverted triangles), and 20°C at 70% field capacity (triangles). Error bars indicate 1 SD and do not appear when smaller than the symbol for the mean. LSD0.05 (Temp x Moisture x Soil x Time) = 0.006.
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Desethylatrazine
In non-adapted soil, DEA concentrations were positively correlated with temperature and moisture (Fig. 4
). Additionally, within temperature and moisture levels, peak DEA concentrations were typically higher and occurred sooner in MS non-adapted soil compared with CO non-adapted soil. Conversely, regardless of temperature, moisture, or time, DEA concentrations in CO and MS adapted soil rarely exceeded the LOQ. Consequently, DEA concentrations in non-adapted soil were typically 3- to 11-fold higher than concentrations in adapted soil, particularly under optimal moisture levels.
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Fig. 4. Desethylatrazine (DEA) concentrations in Colorado (CO) and Mississippi (MS) s-triazine–adapted and non-s-triazine–adapted soil as a function of incubation temperature (10 or 40°C) and soil moisture content (40 and 70% field capacity). Symbols represent the mean of three replications for each of the following treatments: 10°C at 40% field capacity (closed circles), 10°C at 70% field capacity (open circles), 20°C at 40% field capacity (closed inverted triangles), and 20°C at 70% field capacity (triangles). Error bars indicate 1 SD and do not appear when smaller than the symbol for the mean. LSD0.05 (Temp x Moisture x Soil x Time) = 0.003.
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Hydroxyatrazine
The effect of temperature and moisture on HA concentrations differed considerably between CO and MS non-adapted soils (Fig. 5
). Independent of temperature, moisture, and time, the average HA concentration in CO non-adapted soil over the 60-d incubation period was 0.021 µg g–1. In contrast, regardless of temperature or moisture, HA concentrations in MS non-adapted soil increased over the 60-d incubation period, and the highest HA concentrations for all temperature and moisture regimes were observed at study termination, indicating that peak HA concentrations were not yet obtained. Moreover, from 32 d after herbicide application until study termination, HA concentrations in MS non-adapted soil were 1.6- to 3-fold greater at 20°C than at 10°C regardless of moisture level. At 10°C, HA concentrations in MS non-adapted soil were independent of soil moisture. When incubation temperature was increased 10°C, HA concentrations in MS non-adapted soil were greater at 70% FC from 46 d after herbicide application until study termination. Maximum differences in HA concentrations between CO and MS non-adapted soil were observed at study termination when HA concentrations in MS adapted soil were 2.8- to 6.2-fold higher than CO non-adapted soil.
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Fig. 5. Hydroxyatrazine (HA) concentrations in Colorado (CO) and Mississippi (MS) s-triazine–adapted and non-s-triazine–adapted soil as a function of incubation temperature (10 or 40°C) and soil moisture content (40 and 70% field capacity). Symbols for all graphs represent the following treatments: 10°C at 40% field capacity (closed circles), 10°C at 70% field capacity (open circles), 20°C at 40% field capacity (closed inverted triangles), and 20°C at 70% field capacity (open triangles). Error bars indicate 1 SD and do not appear when smaller than the symbol for the mean. LSD0.05 (Temp x Moisture x Soil x Time) = 0.021.
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The effects of temperature and moisture on HA concentrations were drastically different within and across CO and MS adapted soil. For CO adapted soil, moisture was the dominant factor governing HA formation. Peak HA concentrations for CO soil incubated at 40% FC occurred 32 d after application and accounted for at least 34% of the parent compound; moreover, at study termination, HA accounted for approximately 24% of the parent compound. In contrast, peak HA concentrations in CO adapted soil incubated at 70% FC occurred less than 3 d after application in both incubation temperatures, and concentrations were below the detection limit 46 and 16 d after herbicide application in the 10 and 20°C treatments, respectively. For MS adapted soil, peak HA concentrations within all temperature and moisture regimes occurred within 8 d of herbicide application and typically accounted for less than 6.0% of the parent compound's mass. The concentration of HA in MS adapted soil was independent of incubation temperature within 40 and 70% FC treatments, but peak HA concentrations typically occurred sooner and decreased more rapidly at 70% FC than at 40% FC.
Within temperature and moisture regimes, peak HA concentrations were 2.4- to 6.1-fold higher in CO adapted soil compared with MS adapted soil. For adapted soils incubated at 40% FC, HA concentrations in CO soil were 3.1- to 20.9-fold higher than those observed in MS soil over the 60-d incubation. Hydroxyatrazine concentrations in CO and MS adapted soil incubated at 70% FC were similar to the differences observed in HA concentrations between CO and MS adapted soil incubated at 40% FC, yet HA concentrations in CO adapted soil incubated at 70% FC were higher than those observed for MS adapted soil for approximately the first week of the study. From 16 d until study termination, HA concentrations were not different between adapted soils incubated at 70% FC, regardless of temperature regime.
The formation and dissipation of HA across adapted and non-adapted soils differ drastically as a function of temperature and moisture, but some trends were evident. Within temperature and moisture regimes, peak HA concentrations were typically higher, occurred sooner, and declined more rapidly in adapted than non-adapted soil. The exception to this observation was the occurrence and dissipation of HA in CO adapted soil incubated at 40% FC. Independent of time and temperature, HA concentrations in CO adapted soil incubated at 40% FC were higher than MS and CO non-adapted soil.
Rate of 14CO2 Evolution
The rate of 14CO2 evolution from ring-labeled atrazine was not different between CO and MS non-adapted soil with respect to temperature, moisture, or time (Table 3
). Over the 65-d mineralization assay, the average 14CO2 evolution pooled over non-adapted soil, temperature, moisture, and time was 0.004% of applied 14C-atrazine d–1.
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Table 3. The rate of 14C-CO2 evolution from 14C-ring–labeled atrazine in Colorado (CO) and Mississippi (MS) atrazine-adapted (i.e. soils exhibiting enhanced atrazine degradation) and non-adapted soil as a function of temperature (10 or 20°C), moisture (40 or 70% of field capacity [FC]), and time. Values are the mean of three replicates and are expressed as percent of initial ring-labeled 14C-atrazine applied d–1.
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For CO and MS adapted soils, the maximum 14CO2 evolution rate was positively correlated with temperature and moisture. Independent of soil moisture, increasing incubation temperature 10°C in CO and MS adapted soils increased the maximum 14CO2 evolution rate at least 3.6-fold and reduced the lag-phase by 11 d. Similarly, independent of incubation temperature, increasing soil moisture content in CO and MS soils increased peak 14CO2 evolution by at least 2.4-fold and reduced the lag phase by 3 d.
Within all temperature and moisture regimes, 14CO2 evolution rates for MS adapted soil were at least 1.5-fold greater than those obtained for CO adapted soil. Similarly, the lag phase in MS adapted soil was at least 3-fold shorter than CO adapted soil, regardless of the temperature or moisture regime evaluated. Moreover, compared with MS adapted soil, 14CO2 evolution in CO adapted soil was severely impeded at 40% FC across all temperature regimes. For example, at 70% FC, maximum 14CO2 evolution in MS adapted soil was 1.5- and 1.8-fold greater than CO adapted soil at 10 and 20°C, respectively. In contrast, the maximum 14CO2 evolution rate in MS adapted soil was 11.5- and 15.1-fold greater than CO adapted soil at 10 and 20°C, respectively.
With the exception of CO-adapted soil incubated at 10°C and 40% FC, maximum 14CO2 evolution rates for CO and MS adapted soils were greater than those obtained for CO and MS non-adapted soils. Under the optimum temperature and moisture regime, maximum 14CO2 evolution rates in CO and MS adapted soils were 1009- to 1824-fold greater than the maximum 14CO2 evolution rate obtained for CO and MS non-adapted soil pooled over temperature, moisture, and time.
Cumulative 14CO2 Evolution
Cumulative 14CO2 evolution from ring-labeled atrazine did not differ between CO and MS non-adapted soils regardless of temperature, moisture, or time (Fig. 6
). At study termination, the average cumulative 14CO2 evolution from CO and MS non-adapted soil was 0.031% of applied 14C-ring–labeled atrazine.
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Fig. 6. Cumulative 14CO2 evolved reported as percent of total 14C-ring–labled atrazine added in Colorado (CO) and Mississippi (MS) s-triazine–adapted and non-s-triazine–adapted soil as a function of incubation temperature (10 or 40°C) and soil moisture content (40 and 70% field capacity). Symbols represent the mean of three replications for each of the following treatments: 10°C at 40% field capacity (closed circles), 10°C at 70% field capacity (open circles), 20°C at 40% field capacity (closed iverted triangles), and 20°C at 70% field capacity (triangles). Error bars indicate 1 SD and do not appear when smaller than the symbol for the mean. LSD0.05 (Temp x Moisture x Soil x Time) = 2.714.
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Cumulative 14CO2 evolution was positively correlated with temperature and moisture at all sampling dates 4 d after herbicide application in MS adapted soil and 15 d after herbicide application in CO adapted soil. Within adapted soils, the effects of temperature and moisture on cumulative 14CO2 evolution were more pronounced at earlier sampling periods and suboptimal incubation conditions. Increasing soil temperature 10°C in CO and MS adapted soil increased cumulative 14CO2 at study termination at least 3.1- and 1.5-fold when incubated at 40% FC and 70% FC, respectively. Similarly, increasing soil moisture content increased cumulative 14CO2 evolution at study termination at least 1.1- and 2.1-fold when incubated at 20°C and 10°C, respectively.
With the exception of the optimum temperature and moisture regime, cumulative 14CO2 evolution within all temperature and moisture regimes was greater in MS adapted soil than in CO adapted soil from 4 d after herbicide application until study termination. The most notable difference between adapted soils was the effect of soil moisture on cumulative 14CO2 evolution. At study termination, cumulative 14CO2 evolution in MS adapted soil incubated at 40% FC was at least 5.1-fold greater than CO adapted soil regardless of incubation temperature. In contrast, cumulative 14CO2 evolution in MS adapted soil incubated at 70% FC and 10°C was 1.2-fold greater than CO adapted soil, and there was no statistical difference in cumulative 14CO2 evolution between CO and MS adapted soil incubated at optimum temperature and moisture levels.
With exception of CO adapted soil incubated at 10°C and 40% FC, cumulative 14CO2 evolution in CO and MS adapted soils was greater than that of non-adapted soils from 15 d after herbicide application until study termination. Under the optimum temperature and moisture regime, cumulative 14CO2 evolution in adapted soils was 2143-fold greater than the average cumulative 14CO2 evolution of non-adapted soil pooled over temperature, moisture, and time.
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Discussion
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Adapted soils from CO and MS were positive for atzABC and/or trzN, whereas non-adapted soils were not. Thus, the development of enhanced atrazine degradation in CO and MS adapted soil is likely linked to the procurement and/or development of atzABC and/or trzN genes by soil bacteria, thereby allowing them to use atrazine as a N and/or C source. Moreover, the detection of atzABC and/or trzN genes in adapted soil collected from the foothills of the Rocky Mountains and east of the Mississippi river indicates that enhanced atrazine degradation and the occurrence of atzABC and/or trzN genes are likely widespread across the Western and Southern corn-growing regions of the USA, particularly in soils with a history of s-triazine use. Additionally, in adapted soil, the metabolic pathway for atrazine dissipation will likely circumvent traditional biologically mediated N-dealkylation reactions and proceed predominantly through the pathway(s) proposed in Fig. 2. Consequently, the fate and transport of atrazine will likely be different between adapted and non-adapted soils.
Atrazine persistence was significantly reduced in adapted soil. Under the conditions of this experiment, the average atrazine half-life in adapted soil pooled over temperature and moisture was 13-fold lower than non-adapted soil, 10-fold lower than Wauchope's estimate (Wauchope et al., 1992), and 18-fold lower than USEPA's estimate (USEPA, 2006). Because pesticide persistence is a sensitive parameter for accurate modeling of pesticide fate and transport, separate estimates for atrazine persistence are likely needed for adapted and non-adapted soils if accurate atrazine predictions are to be obtained.
Most fate and transport models contain a pesticide submodel that accounts for the effect of soil temperature and moisture on pesticide dissipation in soil (Eq. [1–5]). Based on their review of 148 estimates of Q10 for various pesticides, FOCUS concluded that (i) Q10 does not vary significantly among pesticides; (ii) the mean Q10 for 148 observations is 2.20; and (iii) the 90th and 95th percentile values for Q10 are 2.8 and 3.1, respectively (FOCUS, 1997). Thus, the Q10 value for atrazine in non-adapted soil is within the 90th percentile, but the Q10 estimate for adapted soil is between the 90th and 95th percentiles. Consequently, for modeling atrazine fate and transport in soil as a function of temperature, it may be necessary to use separate Q10 estimates for adapted and non-adapted soils. Conversely, a definitive trend with regard to the effect of moisture on atrazine dissipation between adapted and non-adapted soils was not obtained. FOCUS has recommended that an average β of +0.8 be used to adjust for moisture effects on herbicide dissipation in soil (FOCUS, 1997). This recommendation arose from the observation that variations in measurements of β for individual pesticides are as great as variations between pesticides and that minimal information could be gleaned by calculating β for specific herbicide and soil combinations as opposed to estimating them (FOCUS, 1997). Our data for atrazine dissipation in adapted and non-adapted soil supports this conclusion.
The concentrations of evaluated N-dealkylated metabolites of atrazine were lower in adapted than in non-adapted soil. This observation is likely due to two competing processes: (i) soil bacteria carrying atzABC and/or trzN genes in adapted soil circumvent biologically mediated N-dealkylation reactions, thereby focusing atrazine dissipation primarily through the pathway(s) proposed in Fig. 1, and (ii) DEA and DIA are substrates for atzA and/or trzN, thereby resulting in rapid transformation of any mono-N-dealkylated metabolites to hydroxy–s-triazine intermediates (Seffernick et al., 2000; Shapir et al., 2005). Thus, the formation, concentration, and transport potential of N-dealkylated metabolites of atrazine is lower in adapted than nonadapted soil due to the presence and substrate range of atzABC and/or trzN genes in adapted soil. This observation is significant because USEPA includes the concentrations of all dealkylated metabolites of atrazine in the herbicide's risk assessment (USEPA, 2006). Consequently, if altered metabolic pathways are not accounted for in adapted soils, total s-triazine transport and risk to the environment may be overstated.
Before the discovery of bacteria with atzA and/or trzN genes, the formation of HA in soil was attributed primarily to chemical hydrolysis. Under the classic atrazine dissipation pathway, HA concentrations in aerobic soils rarely, if ever, exceeded 10% of the parent compounds' initial concentration in soil (USEPA, 2006). Consequently, USEPA has not considered HA as a major degradate (USEPA, 2006). However, HA is the obligatory metabolite for the dissipation pathway proposed in Fig. 2, and the conversion of atrazine to HA by atrazine chlorohydrolase (i.e., atzA) is 1010–fold greater than abiotic chemical hydrolysis at pH 7.0 (Wackett et al., 2002; Plust et al., 1981). Thus, in light of HA concentrations in CO adapted soil exceeding 30% of the initial atrazine concentration at suboptimal moisture conditions, HA may need to be reclassified as a major degradate in soils positive for atzA and/or trzN.
Cumulative 14CO2 evolution was greater in adapted than in non-adapted soil, particularly under optimal temperature and moisture regimes. The average cumulative 14CO2 evolution pooled over temperature and moisture was 1287-fold higher in adapted than non-adapted soil at study termination. This observation supports the hypothesis that atzABC and/or trzN genes in adapted soil cause the historic N-dealkylation pathway to be circumvented and/or result in rapid conversion of mono-N-dealklyated metabolites of atrazine to hydroxy–s-triazine intermediates. Moreover, the mineralization data indicate that total s-triazine residues must be lower in adapted than innon-adapted soil due to the greater catabolism in the former. Consequently, the transport potential of atrazine and total s-triazine residues will be lower in adapted than in non-adapted soil.
The detection of atzABC and/or trzN genes in CO and MS adapted soil has significant agronomic implications. Data indicate that enhanced atrazine degradation and atzABC and/or trzN genes are likely widespread across the Western and Southern corn-growing regions of the USA. Soils positive for atzABC and/or trzN may facilitate the development of enhanced atrazine degradation, culminating in a loss of residual weed control. A loss of weed control with atrazine in soils exhibiting enhanced degradation has been demonstrated in MS under laboratory (Krutz et al., 2007) and field conditions (Krutz et al., unpublished). Additionally, the s-triazine herbicides simazine and propazine are substrates for atzA (Seffernick et al., 2000; Shapir et al., 2005). Consequently, soils positive for atzA that exhibit enhanced atrazine degradation will likely be cross-adapted with simazine and propazine. Moreover, the substrate specificity of trzN is wider than that of atzA. Soils exhibiting enhanced atrazine degradation that are positive for trzN will likely be cross-adapted with all commercially available s-triazine herbicides.
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Conclusions
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Genes coding for enzymes able to rapidly catabolize atrazine, and thereby facilitating enhanced atrazine degradation, are likely to be widespread across the Western and Southern corn-growing regions of the USA, particularly in soils with a history of s-triazine use. This phenomenon significantly alters atrazine's persistence in the soil environment. Our data indicate that atrazine's half-life is 10- to 18-fold lower in adapted soil than historic half-life values currently being used as default persistence estimate by modelers (approximately 60 d) and regulatory agencies (approximately 105 d). Additionally, there is a 90% probability that the effect of temperature on atrazine dissipation as measured by Q10 is 1.3- to 1.5-fold greater in adapted soil than the historic Q10 value of 1.9 to 2.2 currently used by modelers and regulatory agencies. Because pesticide persistence is a sensitive parameter for the accurate prediction of pesticide fate and transport, it is likely that current pesticide fate, transport, and risk assessment models would better predict atrazine fate, transport, and risk in adapted soil if shorter half-life values and greater Q10 values are used as input parameters. Additionally, due to the substrate specificity of atzA and/or trzN, the concentration of mono-N-dealkylated metabolites of atrazine will likely be lower in adapted than in non-adapted soil. This is significant because N-dealkylated metabolites of atrazine are included in USEPA's risk assessment. Conversely, hydroxyatrazine is the obligatory metabolite for atrazine dissipation in adapted soils that are positive for atzA and/or trzN, and concentrations exceeded 30% of the parent compounds mass in CO adapted soil under suboptimal conditions. This observation in CO soils may require the USEPA to reclassify hydroxyatrazine as a major metabolite of atrazine in soils positive for atzA and/or trzN. Moreover, because of the substrate specificity of atzA and/or trzN, adapted soils in the Western and Southern corn-growing regions of the USA that are positive for atzA and/or trzN will likely be cross adapted with all s-triazine herbicides, particularly if trzN is detected.
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ACKNOWLEDGMENTS
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Mention of trade names or commercial products in this publication is solely for the purpose of providing specific information and does not imply recommendation or endorsement by the U.S. Department of Agriculture.
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NOTES
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All rights reserved. No part of this periodical may be reproduced or transmitted in any form or by any means, electronic or mechanical, including photocopying, recording, or any information storage and retrieval system, without permission in writing from the publisher.
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TOP
ABSTRACT
INTRODUCTION
