Short-term competition between crop plants and soil microbes for inorganic N fertilizer
Introduction
Intensive agricultural crop production in central Europe largely depends on the input of nitrogen fertilizers, mainly provided in the form of NH4+ or NO3− or a combination thereof. Global estimates indicate that less than ∼50% of the applied fertilizer N are used by the crop, while 2–5% are stored in the soil, ∼25% are emitted to the atmosphere and ∼20% are discharged to aquatic systems (Galloway et al., 2004). In the last decade a wealth of studies have focused on ways to improve fertilizer use efficiency, largely in cereal grain production, and on reducing adverse effects, namely losses of fertilizer N to the environment (Tilman et al., 2002, Mosier et al., 2004). Other studies have focused on fates of N inputs during one or more growing seasons, or on predicting N availability to crops (Jackson et al., 2008).
In agricultural soils plant available N is present in soluble inorganic (NO3−, NH4+, NO2−) and organic N forms. The pool of soluble organic N in unfertilized arable soils can be as large as the mineral N pool and might be strongly involved in mineralization and immobilization processes (reviewed by Murphy et al., 2000). Although dissolved organic N, especially free amino acids, may contribute significantly to plant nutrition in several ecosystems (reviewed by Näsholm et al., 2009), the quantitative importance seems to be negligible (<1%) in agricultural systems that receive high quantities of inorganic N fertilizer (Xu et al., 2008). This indicates that the plant N relations in agricultural soils are predominantly influenced by the rate of mineral N fertilizer application. But not only the amount, also the form of mineral N applied (i.e. NO3− vs. NH4+ vs. NH4NO3) is strongly affecting plant and microbial N metabolism.
In many cultivated soils it has been observed that in plants and microbes NH4+ assimilation exceeds NO3− assimilation (e.g. Azam et al., 1993), which was explained by higher energy costs associated with biological NO3− assimilation (Gutschick, 1981, Smirnoff and Stewart, 1985, Puri and Ashman, 1999). Moreover, it was shown that the presence of NH4+ inhibits NO3− uptake by fungi (Wang et al., 2007) and by plants (Gessler et al., 1998, Gazzarrini et al., 1999, Siddiqi et al., 2002), further promoting plant NH4+ uptake. However, in contrast to these molecular studies, other studies using soils showed in this environment that NH4+ utilization by soil microbes and plants was lower or similar to NO3− utilization (Burger and Jackson, 2003, Song et al., 2007), presumably due to higher mobility of NO3− in soils as compared to NH4+ (Hodge et al., 2000).
One factor leading to these differences in inorganic N assimilation might be that the inorganic N pools in agricultural soils are extremely dynamic (e.g. Jackson et al., 1989), caused by high microbial activities and fertilizer application. Although these dynamics are well established, little is still known about the mechanisms and short-term effects (hours to days) of different ratios of NH4+:NO3− on microbial N transformation processes. As some of these processes lead to N losses to the environment (e.g. leaching of NO3− or N gas emissions caused by nitrification or denitrification), even short-term increases in microbial activity can negatively affect the fertilizer use efficiency of crop plants.
Besides the availability of inorganic N, competition with soil microbes is one of the most critical factors affecting the ability of plants to acquire N from soil (Kaye and Hart, 1997). In several short-term 15N tracer studies (up to several days) investigating grassland ecosystems, microbes often assimilated more 15N-labelled inorganic N than plants did, but after an initially rapid N capture, microbial biomass appeared to reach a steady state, probably because of insufficient available C to maintain the fast initial growth rates (Hodge et al., 2000, Harrison et al., 2008). The same studies showed that during the following period, microbial 15N was gradually released by microbial decay and remineralization into the soil, eventually becoming available for plant root uptake. After longer time periods (weeks to months), plants contained an increasing proportion of the added 15N, showing that plants indeed utilized this N resource (Harrison et al., 2007). In other words, the turnover rate of plant biomass was much slower than that of microbes, which allowed plants to compete for the same N for extended periods, therefore enhancing plant competitiveness for N.
However, in high N ecosystems, like in agricultural soils, it was suggested that competition could be less severe (Schimel and Bennett, 2004), though plants and microbes are considered to compete for any available N, particularly for NH4+ and NO3−. Further, besides competition between plants and soil microbes, competition among different groups of soil microbes for fertilizer N is of considerable importance. Burger and Jackson (2003) found that, due to the high availability of inorganic N after fertilization, competition between plants and heterotrophic microbes for NH4+ markedly decreased and nitrification became the major fate of NH4+. Over time, the N economy in well-aerated agricultural soils therefore becomes progressively NO3− dominated and plants cover their N-demand from mainly NO3− (Schimel and Bennett, 2004). However, it still remains unclear to which degree short-term (hours to days) competition for fertilizer N between plants, heterotrophic and autotrophic microbes is affected by the form and amount of mineral N applied.
The main objectives of the present study therefore were to assess (1) the effect of applied inorganic N form on the degree of competition for fertilizer N between crop plants and soil microbes, (2) the population response of bacteria and fungi to the different N treatments, as determined by estimation of gene copy numbers (quantitative PCR), (3) preferences in uptake of NH4+ or NO3− by plant roots and soil microbes as well as possible inhibitory effects of one N form on uptake of the other form and (4) fertilizer induced changes of microbially mediated N transformation rates that control N distribution to the different soil compartments as well as losses of fertilizer N to the environment.
Section snippets
Soil sampling and experimental setup
Soil was collected in April 2006 from two sites in the vicinity of Vienna, Austria, namely from Purkersdorf and Niederschleinz. Soils from both sites are widely distributed and are frequently used for barley cultivation in this area. A detailed summary of site characteristics and soil properties is given in Table 1. Soil samples (each ∼25 kg) were collected from 0 to 20 cm depth from both sites and immediately stored at 4 °C until further analysis. Prior to the start of the experiments soils
Plant and microbial biomass and microbial community composition
Plant biomass significantly increased during 8 d in both soils in all fertilizer treatments (Fig. 1). During the first 2 d after N fertilization, however, there was no significant difference in plant biomass between applied N forms and between soils (one-way ANOVA, P > 0.05). After 3 d plant biomass was significantly lower in both soils in the NH4Cl treatment compared to NH4NO3 and KNO3 as N source. This difference became stronger until the end of the experimental period and at the last
Fertilizer N uptake by plants and soil microbes
A major goal of the present study was to assess the intensity of competition for inorganic N between barley plants and soil microbes in two agricultural soils, and its dependence on the form of applied fertilizer N. We found that 8 d after N application crop plants were the major sink for inorganic fertilizer N in both soils. At this time 45–80% of initially applied 15N fertilizer was recovered in the plants compared to only 1–10% recovered in soil microbial biomass, proving that plants were
Acknowledgements
This work was supported by Project LS-05-36 by Vienna Science and Technology Fund WWTF to a project consortium headed by PIs JS, WW and SZ. The authors thank Dr. Konrad Fiedler for statistical advice and one anonymous reviewer for valuable comments to improve the manuscript.
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