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a USDA–ARS, Northwest Irrigation and Soils Research Laboratory, 3793 N. 3600 E., Kimberly, ID 83341
b Dep. of Chemistry, Queen Mary, University of London, London E1 4NS, UK
c Soil, Plant, and Ecological Sciences Division, P.O. Box 84, Lincoln University, Canterbury, New Zealand
* Corresponding author (bturner{at}nwisrl.ars.usda.gov)
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONCONCLUSIONSREFERENCES |
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phosphate of organic polyphosphates. Some orthophosphate diesters, notably RNA and phosphatidyl choline, degraded rapidly to orthophosphate monoesters in NaOH–EDTA although DNA, other phospholipids, and orthophosphate monoesters were more stable. Changes in probe temperature had a marked influence on signal intensities and the relative magnitude of signals from orthophosphate monoesters and inorganic orthophosphate, and we suggest that solution 31P NMR spectroscopy of soil extracts be performed at 20°C. |
INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONCONCLUSIONSREFERENCES |
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Detailed information on soil P composition can be obtained by alkaline extraction and solution 31P NMR spectroscopy. This procedure was first used by Newman and Tate (1980) to investigate P in New Zealand grassland soils, since when it has become the method of choice for determining soil P composition (e.g., Hawkes et al., 1984; Adams and Byrne, 1989; Condron et al., 1990; Bedrock et al., 1994; Guggenberger et al., 1996; Makarov et al., 1997; Mahieu et al., 2000; Amelung et al., 2001). Solution 31P NMR has clear advantages over conventional soil P fractionation schemes, which provide no structural information, while the ability of 31P NMR to distinguish between similar compounds in complex matrices obviates the need for the lengthy sample clean-up and separation procedures involved in chromatography (Anderson and Malcolm, 1974). The extraction procedure can also be improved using a combination of 0.25 M NaOH and 0.05 M EDTA, which recovers a greater amount and range of soil P compounds than other extractants (Cade-Menun and Preston, 1996). First proposed by Bowman and Moir (1993), NaOH–EDTA extraction is now used to study P in soils (Dai et al., 1996; Robinson et al., 1998; Cade-Menun et al., 2002; Turner et al., 2003), animal manures (Crouse et al., 2000), and aquatic sediments (Sundareshwar et al., 2001).
Identification of compounds by solution 31P NMR is based on their chemical shift relative to an external H3PO4 standard. Chemical shift is defined by:
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In the absence of a comprehensive reference for chemical shift assignments, the principal objective of this study was to determine the chemical shifts of a wide range of P compounds in a soil NaOH–EDTA extract matrix as a reference for future solution 31P NMR studies of soils and sediments. Secondary objectives were to examine the degradation of P compounds during solution 31P NMR analysis and investigate the effects of probe temperature on spectral quality.
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MATERIALS AND METHODS |
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Bacteria were cultured from an upland blanket peat from the Upper Teesdale National Nature Reserve, County Durham, UK (32% total C, 0.6% total P, pH 3.9). Soil suspensions (1 g of soil and 10 mL of deionized water, shaken gently for 5 min) were spread thinly on standard agar plates (containing inorganic P) and incubated for 14 d at 30°C. Bacteria were scraped from the agar and added directly to rehydrated soil extract.
For solution 31P NMR spectroscopy, freeze-dried soil extract (approximately 500 mg) was redissolved in 5 mL of 1 M NaOH and 0.5 mL of D2O (for signal lock) and spiked with model compound (1–15 mg) or bacteria (24 mg). Redissolving the freeze-dried extract in 1 M NaOH ensures consistent chemical shifts and optimal spectral resolution by maintaining a solution pH >12. Occasional P compounds were dissolved directly in D2O and NaOH only (i.e. no soil extract).
Solution 31P NMR spectra were obtained using a Bruker AMX 600 spectrometer (Bruker, Germany) operating at 243 MHz with a 5-mm probe. We used a 30° pulse width, a total acquisition time of 1.5 s (pulse delay 0.808 s, acquisition time 0.673 s) and broadband proton decoupling (additional spectra were acquired for some samples without proton decoupling). The delay time used here allows sufficient spin-lattice relaxation between scans for P compounds in NaOH–EDTA, confirmed by a recent detailed study of relaxation times for P compounds in various soil extractants (Cade-Menun et al., 2002). Temperature was regulated at 24°C. Between 80 and 400 scans were collected to obtain acceptable signals. Chemical shifts were measured relative to an external standard of 85% H3PO4 after Lorentzian convolution with a width of 10 Hz. We used the deconvolution process of the Bruker WinNMR program to determine chemical shift, line width, and area of individual signals. Spectra were plotted using a line broadening of 5 Hz. Spectra were collected immediately after preparation (usually within 1 h) and repeated at intervals during storage at room temperature to determine degradation, with the same number of scans collected each time. No degradation was observed unless specified.
The effect of probe temperature on solution 31P NMR spectra was investigated by analyzing (i) a synthetic mixture of model P compounds, and (ii) the soil NaOH–EDTA extract. Probe temperature was varied between 19 and 44°C for the synthetic mixture and between 18 and 37°C for the soil extract. Spectra were recorded for 128 scans (synthetic mixture) or 1024 scans (soil extract), with other machine parameters as described above.
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RESULTS |
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Orthophosphate monoesters gave signals between 3 and 6 ppm (Table 2, Fig. 2) , and did not degrade in NaOH–EDTA. Myo-inositol hexakisphosphate (phytic acid) gave four characteristic signals in the ratio 1:2:2:1 at 5.85, 4.92, 4.55, and 4.43 ppm, corresponding to the positions of the P atoms on the inositol ring (Costello et al., 1976; Fig. 2). Other orthophosphate monoesters resonated in this region, including sugar phosphates (glucose phosphates at 3.39 and 5.36 ppm), mononucleotides (4.32 to 4.78 ppm) and the monoester breakdown products of phospholipids (choline phosphate at 4.05 ppm, ethanolamine phosphate at 4.71 ppm). The only orthophosphate monoester signals not in the 3 to 6 ppm region were aromatic monoesters (see below) and phosphoenolpyruvate (0.25 ppm), a common compound in plant material. The samples of adenosine and guanosine 5' monophosphate also gave small signals between 12 and 14 ppm, which may indicate contaminant aromatic phosphonic acid esters (see below). Lower inositol phosphate esters (inositol mono- to pentakisphosphates) and isomeric forms other than myo (scyllo, D-chiro, neo) also occur in soils and sediments (Turner et al., 2002b), but were not analyzed because of their expense. However, the lower inositol phosphate esters almost certainly give different signals to those of myo-inositol hexakisphosphate (Kemme et al., 1999).
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Phosphonates, which contain a C–P bond, gave signals between 12 and 23 ppm (Table 4, Fig. 4) . Aminoethyl phosphonates gave signals around 20 ppm (Newman and Tate, 1980), while aromatic phosphonic acid esters (which contain both a phosphonate and an ester bond) appeared between 12 and 14 ppm. Phosphocreatine, which contains a P–N bond rather than a P–C bond as in the phosphonates, gave a signal at 0.29 ppm. No degradation of aminoethyl phosphonic acids was detected during several months storage in NaOH–EDTA, but a compound with a chemical shift of 12.07 ppm appeared after 24 h in the ß-naphthyl phenyl phosphonate solution, and increased to the height of the signal from the original compound after storage for 15 d, despite no change in the height of the original signal. Similar weak signals were detected between 12 and 13 ppm in the sample of adenosine 5' monophosphate (Table 2). When a spectrum of 2-aminoethyl phosphonic acid was acquired without proton decoupling, the signal split into seven smaller signals (Fig. 4).
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phosphates, respectively. Similarly, ATP gave signals at -4.28, -9.68, and -19.68 ppm, corresponding to the 
, , and ß phosphates, respectively.
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DISCUSSION |
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Orthophosphate monoesters are the major functional class of organic P in most soils, of which the higher inositol phosphates are usually dominant (Turner et al., 2002b). However, the complex signals from myo-inositol hexakisphosphate make it difficult to quantify this compound using solution 31P NMR spectroscopy. Despite this, it may be possible to discriminate among the range of compounds present in the orthophosphate monoester region using spectral deconvolution software, although this will require the acquistition of well-resolved spectra. The most readily identified orthophosphate monoesters are glucose-1-phosphate (3.39 ppm) and choline phosphate (4.05 ppm), because of their separation from the main body of signals between 4.3 and 6.0 ppm. Choline phosphate has been previously reported at 4.3 ppm (Adams and Byrne, 1989) and 3.56 ppm (Newman and Tate, 1980), but this is almost certainly accounted for by differences in pH. Adams and Byrne (1989) reported similar chemical shifts to those reported here for glucose-6-phosphate (5.30 ppm) and glycerophosphate (4.78 ppm) in alkaline extracts.
Orthophosphate diesters dominate organic P inputs to the soil from plants and microbes, but are rapidly degraded upon release and typically represent only a small proportion of the soil organic P (Anderson, 1980). Signals from the orthophosphate diesters are commonly grouped together as a single functional class of organic P, but we found reasonable resolution among the various compounds. For example, signals from DNA (-0.37 ppm) and alkali-stable phospholipids (1.5 to 1.8 ppm) were clearly distinguishable. Among the phospholipids, signals from phosphatidyl ethanolamine (1.75 ppm) and phosphatidyl serine (1.56 ppm) were well resolved from phosphatidyl choline (0.78 ppm). The latter may interfere with signals from RNA, although both these compounds were rapidly degraded in alkaline solution (see below). Signals between 0 and 1 ppm were previously assigned to teichoic acids (e.g., Condron et al., 1990), which are present in the cell walls of gram-positive bacteria and are also produced by some actinomycetes (Naumova et al., 2001). However, teichoic acids were recently measured at 1.9 ppm in delipidized extracts of the gram-positive bacteria Bacillus subtelis (Makarov et al., 2002), suggesting that they do not contribute greatly to the observed signals in the orthophosphate diester region of alkaline soil extracts. This is possible, because bacterial walls are assembled from P-free teichuronic acid units in P-limited environments (Stewart and Tiessen, 1987).
Organic and inorganic polyphosphates both gave similar signals in the negative region of the spectra, but can be differentiated by the presence or absence of an intermediate signal around -9 ppm from the phosphate group of the organic polyphosphates. The chemical shifts reported here for inorganic polyphosphates are similar to literature values for inorganic polyphosphates in alkaline solution, with terminal P groups at approximately -4 ppm and mid-chain P groups giving signals in the -20 ppm region (Adams and Byrne, 1989; Glonek et al., 1975). The high degree of peak splitting in the inorganic polyphosphate spectrum is due to homonuclear spin-spin coupling induced by the interaction of P nuclei in close proximity.
The spectrum of 2-aminoethylphosphonic acid acquired without proton decoupling highlights the importance of decoupling in the analysis of soil extracts by solution 31P NMR spectroscopy. The splitting results from heteronuclear spin-spin coupling between 1H and 31P nuclei, which is removed by exciting both nuclei simultaneously. Without proton decoupling, splitting of weak signals from trace amounts of compounds such as phosphonates may result in such compounds being undetected in poorly resolved spectra.
Binaphthyl phosphate is the aromatic diester reported at 7.2 ppm by Bedrock et al. (1994). This appeared slightly downfield of signals from an unidentified compound at 6.9 ppm in soil NaOH–NaF extracts (Amelung et al., 2001), but suggests the presence of an aromatic orthophosphate diesterin these samples. However, other aromatic orthophosphate diesters did not give similar signals. Notably, aromatic phosphatase substrates gave widely different signals to most natural phosphate esters, suggesting substantial differences in the chemical environment around the P groups of these structurally different compounds. This has implications for the determination of phosphatase activity, because the enzymes may behave differently toward such aromatic compounds compared with those constituting the bulk of the organic P inputs to the soil. For example, snake venom phosphodiesterase has more than four times the hydrolytic activity toward DNA than bis-para-nitrophenyl phosphate (Turner et al., 2002a).
Degradation of Phosphorus Compounds
Orthophosphate diesters were susceptible to degradation in NaOH–EDTA, but the extent of this varied among the different compounds. For example, the complete hydrolysis of RNA to orthophosphate monoesters within 24 h was in marked contrast to the stability of DNA (Anderson, 1967; Makarov et al., 2002). This atleast partly explains the dominance of a signal close to 0 ppm in the orthophosphate diester region of most alkaline soil extracts (e.g., Newman and Tate, 1980; Adams and Byrne, 1989). Of the phospholipids, phosphatidyl choline was the most readily degraded, with almost complete conversion to orthophosphate monoesters within 24 h. Phosphatidyl choline appeared to degrade to glycerophosphate (4.81 ppm) and phosphatidic acid (5.15 ppm), rather than choline phosphate (4.05 ppm). Phosphatidyl serine degraded much more slowly, and phosphatidyl ethanolamine showed no degradation in 24 h. This agrees with the stability of these compounds during 24 h in molar NaOH (Brannon and Sommers, 1985), and suggests that they are responsible for signals between 1 and 2 ppm in the region of alkaline soil extracts. Aromatic orthophosphate diesters also degraded slowly to aromatic orthophosphate monoesters in alkaline solution (Browman and Tabatabai, 1978).
The rapid degradation of some orthophosphate diesters in alkaline solution is an unavoidable limitation on the quantification and characterization of soil organic P, because alkaline solutions are required to extract organic P from most soils (Anderson, 1980). Strong-acid extraction techniques can extract large proportions of organic P from some soils (Bowman, 1989), but are unsuitable for subsequent 31P NMR analysis without additional treatment. Therefore, the degradation of some compounds must be accepted as an artifact of soil organic P analysis by current procedures. Given the rapid nature of the degradation of RNA and phosphatidyl choline, it seems probable that most degradation will occur during extraction and lyophilization. Therefore, the possibilities to reduce this are limited, although the rehydration of freeze-dried extracts immediately before NMR analysis is advisable. It is possible that the nature of orthophosphate diesters in the soil (such as in complexes with humic material), may limit their degradation in alkaline solution, but this seems unlikely, at least for RNA (Makarov et al., 2002). Many orthophosphate diesters are derived from soil microbes, which can represent a considerable proportion of the soil organic P (Turner et al., 2001b), so the greatest errors may occur in soils high in microbial biomass.
Based on the chemical shifts of orthophosphate diesters, and their relative degradation in alkaline solution, we suggest that the orthophosphate diester region of solution 31P NMR spectra of alkaline soil extracts can be reclassified into three groups of compounds: (i) DNA between -1.0 and 0 ppm, (ii) alkali-labile diesters (RNA and phosphatidyl choline) between 0 and 1.0 ppm, and (iii) microbial phospholipids between 1.5 and 1.8 ppm. In addition, teichoic acids may also be identified at approximately 1.9 ppm in extracts of some soils (Makarov et al., 2002). This refines peak assignments and will enhance the information obtained from solution 31P NMR spectroscopy of alkaline soil extracts. The assignments were confirmed by the presence and degradation of orthophosphate diesters in soil bacteria corresponding to RNA (0.54 ppm), DNA (-0.28 ppm), phosphatidyl serine (1.56 ppm), and phosphatidyl ethanolamine (1.66 ppm).
Organic and inorganic polyphosphates were stable in NaOH–EDTA, suggesting that their absence in alkaline soil extracts is not explained by degradation during analytical procedures. Long-chain polyphosphates degrade to shorter chain lengths in the presence of metal ions in sediment extracts (Hupfer and Gächter, 1995), but degradation is slowed when EDTA is included in the initial extract. This is probably due to the complexation of free metals, and confirms the suitability of NaOH–EDTA as an extractant for soil polyphosphates (Cade-Menun and Preston, 1996).
Two signals are sometimes detected in the 20 ppm region of soil extracts, probably representing a compound such as 2-aminoethyl phosphonic acid around 21 ppm and a higher molecular weight phosphonolipid (e.g., phosphonylethanolamine) around 19 ppm (Newman and Tate, 1980). Degradation of the latter to an alkyl phosphonate has been reported in alkaline solution (Newman and Tate, 1980; Cade-Menun et al., 2002). We detected no degradation of aminoethyl phosphonic acids in NaOH–EDTA, but we did not include a phosphonolipid in our experiments.
Effect of Probe Temperature on Phosphorus-31 NMR Spectra
Small changes in chemical shifts of signals from organic P compounds in response to temperature changes are widely reported and, at least for orthophosphate diesters, appear to be linked to conformational changes (Gorenstein, 1984). However, increases in temperature can also influence spin-lattice relaxation times (T1 times), which may explain the decreases in signal intensity with increases in temperature (Crouse et al., 2000). For a 31P NMR experiment to be quantitative, the pulse delay time must be sufficient to allow nuclei to fully relax following excitation (Cade-Menun et al., 2002). If nuclei fail to fully relax (pulse delay < T1), which may occur as temperature increases, then signal intensities will be smaller than for fully relaxing nuclei. Changes in the relative intensities of orthophosphate monoesters and inorganic orthophosphate add further complication. Therefore, we suggest that solution 31P NMR experiments should be conducted at a standardized temperature close to 20°C, as suggested elsewhere (Crouse et al., 2000; Cade-Menun et al., 2002). This will ensure comparability among studies, reduce the number of scans required to obtain acceptable signals, and minimize temperature-associated degradation of compounds.
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CONCLUSIONS |
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phosphate group of ADP and ATP. Some orthophosphate diesters degrade in the alkaline conditions used to extract and analyze soil organic P, notably RNA and phosphatidyl choline, which may limit the accurate determination of soil P composition by solution 31P NMR spectroscopy. However, other compounds, including DNA and microbial phospholipids, are more stable, at least in the time frame of 31P NMR experiments. Relative signal intensities from inorganic orthophosphate and orthophosphate monoesters vary with probe temperature, so a standard operating temperature of 20°C is recommended for solution 31P NMR analysis. |
ACKNOWLEDGMENTS |
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Received for publication May 10, 2002.
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