Gross nitrogen mineralization-, immobilization-, and nitrification rates as a function of soil C/N ratio and microbial activity
Introduction
The low concentration of NO3− found in forest soils has often been attributed to low rates of nitrification (Vitousek et al., 1982, Gosz and White, 1986). This interpretation is supported by observations of low net nitrification rates during incubation assays of soil samples. However, occasional measurements of gross nitrification suggest a rapid turnover of a small NO3− pool in forest soils, and that the dominant fate of NO3−, as well as NH4+, is immobilization in the soil organic matter pool (Davidson et al., 1992, Groffman et al., 1993, Stark and Hart, 1997). In this way, immobilization may prevent nitrogen leakage to ground and surface waters.
The extent of immobilization varies between 35 and 95% from one soil to another (Mead and Pritchett, 1975, Heilman et al., 1982, Melin et al., 1983, Schimel and Firestone, 1989, Hart and Firestone, 1991, Hart et al., 1993). Nitrogen is immobilized either by abiotic or biotic processes. Fixation of NH4+ to clay minerals is fast (<30 min) but usually less than 10% of the added NH4+ is fixed (Drury and Beauchamp, 1991, Trehan, 1996). Most of the immobilization to the soil organic matter is biotic. Early work estimated soil microorganisms to be responsible for 10–50% of NH4+ immobilization (Brookes et al., 1985) and more recent analyses by NMR of the organic matter of 15NH4+ or 15NO3− treated soils found the organic 15N in microbially derived peptides and proteins (>80%), nucleic acids, and aliphatic amine groups after several months of in situ incubation (Clinton et al., 1995). The average turnover time of N in microbial biomass is estimated to 1–2 months (Davidson et al., 1992), but some of the immobilized N becomes very stable (Kelley and Stevenson, 1985), as a result of fixation by 2:1 clay minerals (van Veen et al., 1985, Breitenbeck and Paramasivam, 1995), repeated cycles of immobilization and mobilization (Jansson and Persson, 1982, He et al., 1988), and accumulation of persistent residues of microbial cells (Paul and Juma, 1981).
Despite the obvious importance of soil microorganisms in the turnover and retention of nitrogen in forest soils, the causes of variation of immobilization of N from one soil to another and between abiotic and biotic processes are not well known. Some observations suggest that the immobilization is controlled by the concentration of available C (Woodmansee and Duncan, 1980), and others that it is inversely dependent on the amount of available inorganic N (Priha and Smolander, 1995, Bengtsson and Bergwall, 2000).
Mineralization of soil N depends on a wide range of factors, including the C/N-ratio (Frankenberger and Abdelmagid, 1985), the N content (Iritani and Arnold, 1960), lignin content (Frankenberger and Abdelmagin, 1985, De Neve et al., 1994), water soluble N and cellulose content (Iritani and Arnold, 1960, Bending et al., 1998) of the litter, the light fraction organic matter of the soil (Janzen et al., 1992, Sierra, 1996), microbial respiration and ATP content (Alef et al., 1988), microbial biomass (Dalal and Meyer, 1987), and microbial N content (Fisk and Schmidt, 1995). The diversity of factors correlated with N mineralization reflects the variation in substrates and microbial communities being used and temporal changes in substrate quality.
Models predicting nitrogen turnover and retention in soils often include the C/N ratio as an important factor in determining the rate of mineralization, immobilization and nitrification (van Veen et al., 1984, Aber, 1992, Bradbury et al., 1993, Janssen, 1996). The idea to use the soil C/N ratio to predict variations in N mineralization and immobilization rates among soils is based on the fact that heterotrophic soil bacteria usually have a lower C/N ratio than the soil they inhabit. If it is assumed that the cells have a C/N ratio of 10 and respire about 50% of their C uptake, they may be N limited above a soil C/N ratio of 20 and C limited below (Tate, 1995). Soils with a high C/N ratio may then be characterized by rapid immobilization of N and soils with a low C/N ratio by slower N immobilization and a surplus of available NH4+, derived from deamination of organic carbon sources.
The evidence for a correlation between the soil C/N ratio and nitrogen immobilization and mineralization is equivocal, at least partly because early work was confined to measurements of net rates of N transformation. Within-site variations of the C/N ratios of different pools of organic matter and between-site variations of the C and N assimilation efficiency of the microbial biomass may also confound the usefulness of the soil C/N ratio to predict gross nitrogen transformation rates. Therefore, we designed a 15N pool dilution experiment to simultaneously measure gross immobilization, mineralization, and nitrification, in an effort to challenge the hypotheses of a positive relationship between the C/N ratio and N immobilization and a negative relationship between the C/N ratio and N mineralization and nitrification in three forest soils. Even if the soil C/N ratio may prove useful to predict site-to-site variations of the N transformations, temporal variation of soil temperature and moisture will trigger dynamics of microbial biomass and activity that influence N transformations more than the spatial variation of the C/N ratio. Therefore, we developed the sub-hypothesis that the variation in N transformation rates is controlled by the variations in microbial biomass and activity—a high biomass and activity would correspond (1) to high rates of N immobilization and mineralization, and, as nitrifiers tend to be competitively inferior to heterotrophs (Verhagen and Laanbroek, 1991, Verhagen et al., 1995), (2) to low nitrification rates.
It is well established from laboratory experiments that soil drying and rewetting may bring about a flush of C and N mineralization (Birch, 1958, Agarwal et al., 1971, van Gestel et al., 1991) and an increase in microbial numbers and activity (West et al., 1986). The origin of the mineralized N may be both biomass lyzed by the drying, and non-biomass organic matter that becomes more accessible to microbial attack after drying and rewetting (Jager and Bruins, 1975, Marumoto et al., 1982). We used this evidence to test the sub-hypothesis and induced a microbial growth phase by drying and rewetting the three soils, and then evaluated the subsequent gross N transformations rates. Although short-time laboratory 15N pool dilution experiments do not necessarily reflect N transformation rates in the field, they facilitate experimental manipulations and help explaining mechanisms causing variation in N transformation rates from one soil to another.
Section snippets
Soil sampling
Soil material was collected from deciduous forests in southwestern Sweden in July 1998. Soil I was found in the vicinity of Maglö (56 °3′N, 13 °12′E), and Soil II and III were found in Torup (55 °33′N, 13 °37′E). After removal of the litter, five samples of the top 5 cm of the soil were collected randomly within a 20 by 20 m square. The samples were sieved through a 4 mm mesh and then pooled. Remaining roots and leaf pieces were removed by hand and the soils were left to air-dry at room temperature
Gross nitrogen transformation rates
The high rates of mineralization and immobilization during day 1–2 and 3–4 were preceded by a burst of microbial activity and then followed by lower rates as the incubation of the soils proceeded (Fig. 1, Fig. 2, Table 2). This pattern coincided in general with the one hypothesized when the experiment was designed, but no significant relationships were found between the gross mineralization and immobilization rates and the microbial biomass/activity in the soils (Table 3, Table 4) due to 1–2
Discussion
Rather than supporting the assumption that the soil C/N ratio controls potential gross immobilization and mineralization and explains differences in their rates from one soil to another, this study suggests that differences in respiration rate and ATP content are more indicative of the magnitude of the two processes. The soil with the high C/N ratio (Soil III) complied with a number of criteria for high immobilization rates, such as low in situ concentrations of extractable NO3− and NH4+ and
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