1. Sequence of processes for nutrient acquisition by occupation of new soil volume
The N uptake by roots is not even throughout the rooted soil volume and along the roots. The main uptake occurs in the root hair zone (Waisel et al., 2002), c. 1–5 cm behind the root tip (Fig. 1). The zones behind the root hairs are responsible for only minimal nutrient uptake and are not considered here. Therefore, when a new soil volume is occupied, the duration of N uptake in the individual zones is limited by the passage in the root from the root tip to the root hair zone and just behind it (Clarkson, 1985; Ingestad & Ågren, 1988). The distance from the root tip to the end of the root hair zone is c. 1–5 cm, and roots grow from 0 to 2 cm d−1. This limits the period of direct N uptake from newly occupied soil to a few days (Thaler & Pagès, 1998).
Figure 1. Microbial processes along the growing root and released rhizodeposits. The competition for nitrogen (N) between roots and microorganisms peaks at periods of strong microbial growth. Strong root–microorganism competition for N as well as stimulation of microbial activity by easily available rhizodeposits accelerates the decomposition of soil organic matter (SOM) for additional N mineralization (real priming effect). The time line on the right represents the period after the root occupies new soil volume. The microorganism (MO) density is presented as changes compared with root-free soil. Compilation from Kuzyakov (2002) and Dennis et al. (2010).
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Generally, root hairs have a life span of a few days, although they may persist for longer periods, particularly in grasses (Mengel et al., 2001; Gregory, 2006). During root growth, different root zones release rhizodeposits of different compositions (Fig. 1). Although roots might take up some of the released organics (mainly low-molecular-weight organics; Näsholm et al., 1998, 2009; Kuzyakov & Jones, 2006; Biernath et al., 2008; Hill et al., 2012), a substantially greater release than uptake results in a net release. When root hairs die and lyse, this C also contributes to rhizodeposition. Most of the C released as rhizodeposition is readily available, and microorganisms use this C for growth. Microbial utilization of rhizodeposits is very fast and occurs within a few hours for exudates (Jones & Kielland, 2002; Jones et al., 2005; Kuzyakov & Jones, 2006; Kemmitt et al., 2008; Fischer & Kuzyakov, 2010; Fischer et al., 2010) and a few days for sloughed-off cell walls and root hairs (Dormaar, 1992).
Considering these short utilization periods and the turnover time of rhizosphere microorganisms ranging from days to weeks (Staddon et al., 2003; Schmidt et al., 2007; Blagodatskaya et al., 2011), we assume that the excess of easily available C is depleted within a few days via microbial uptake, utilization, and decomposition. This causes the microorganisms that were previously growing on the excess of substrate to starve. This absence of new C input and continuous consumption of C in the microorganisms leads to the release of N immobilized in microbial biomass into the soil. This process sequence results (Fig. 2) in the availability of N for plants.
Figure 2. Sequence of processes when ingrowing roots occupy new soil volume and during interactions between roots and microorganisms for carbon (C) and nitrogen (N) uptake. Despite the initial uptake of N mineralized from soil organic matter (SOM) by microorganisms (MO), their much shorter life cycle compared with that of plant roots leads to the release of acquired N back into the soil; this mineral N is then available for root uptake. Nmin, mineralized N. See text for further explanation.
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As described in the sequence of processes involving the competition between plants and microorganisms for available N, the microorganisms stimulated by available C begin capturing N earlier than the roots (vertical arrow, right, in Fig. 2). This leads to a temporary decrease in the available N for the roots, and this N limitation in turn stimulates them to release additional C (Merckx et al., 1987; Liljeroth et al., 1990; Kuzyakov et al., 2001). Although the mechanisms underlying the stimulation of C release by roots as a result of N limitation remain unclear, the increase in C is associated with the development of more abundant fine roots, and consequently higher rhizodeposition. Clarifying the C release by roots as a result of N limitation could significantly contribute to our understanding of mutualistic mechanisms, that is, whether they occur at the level of the root system or individual roots.
Following the uptake of root exudates, microorganisms use the C for growth and maintenance respiration. As N is limited even for microorganisms, they produce certain extracellular enzymes for the mineralization of poorly available C sources, such as SOM, to obtain N (Schimel & Weintraub, 2003; Manzoni et al., 2012). These depolymerizing extracellular enzymes are glycosidases, phenoloxidases, peroxidases, glucosaminidases, and peptidases (Blagodatskaya & Kuzyakov, 2008), which break down polymers and generate dimers and monomers that are soluble and available for microbial uptake (Hill et al., 2012). Because microbial turnover in the rhizosphere is very rapid (a few days), the C losses by respiration are very high. Consequently, these microorganisms become energy-starved and obtain their energy from amino acids. Microorganisms strip off the N from the amino acids, thereby making the C skeletons available for the tricarboxylic acid (TCA) cycle for energy and growth. Finally, is released as a metabolite in this process (ammonification). This form of N can be absorbed by roots. Importantly, the net N release from starving or dying microorganisms is higher than the initially available N content because of microbial mining for extra N from SOM during root growth. Clarholm (1985) suggested another mechanism of N release from microorganisms that involves microbial grazing by soil animals, and which is particularly important in the rhizosphere (described in detail by Bonkowski et al., 2009).
2. Effect of time on the nutrient flow direction
Two factors contribute to the redistribution of N after its initial acquisition by microorganisms and roots (Figs 1, 2): N flow direction, and life cycle duration of rhizosphere microorganisms and plants. The N flows driven by competition between roots and microorganisms are directed to the roots (Fig. 2). Decomposition of SOM by some exoenzymes releases minerals and amino acids and some amino sugars, which can be acquired by microorganisms and, after mineralization to or , by roots. Amino acids can also be used directly by roots, although compared with microorganisms, plant roots are often not very efficient competitors for this N source. As shown in Fig. 2, at the initial stage, microorganisms outcompete roots for inorganic N because of rapid growth rates and high surface-area-to-volume ratios compared with those of root hairs (Rosswall, 1982). Thus, even in soils with a high density of roots, for example in the upper 5 to 10 cm in grassland, most N will be allocated to microorganisms shortly after N addition or release from decomposing litter. This reduces N leaching losses as a result of the limited uptake capacity of roots.
At this stage, the second factor responsible for redistribution of N between microorganisms and roots arises: the duration of the life cycle of rhizosphere microorganisms and roots. The turnover time of the microorganisms is very short (a few days; Schmidt et al., 2007) because of high C losses by respiration. In microorganisms, the C released as CO2 is lost, and their C:N ratio decreases. Despite this, the microbial C:N ratio is stable and ranges between 5 and 10 (average, c. 8; Cleveland & Liptzin, 2007). Mineral N is thus again available for microorganisms and roots. This cycle of the uptake and release of mineral N (and amino acid N) occurs within a few days according to the life cycle of the rhizosphere microorganisms.
Unlike the N flow in microorganisms, the net N flow to and in the roots is unidirectional. Despite some evidence for N rhizodeposition (Wichern et al., 2008), the net N flow is directed to the roots, except in symbiotic diazotrophs. Although, in diazotrophy, the net flow of the sum of N species is directed to the roots, the minor efflux of the combined N obtained from the plant is offset by the influx of N generated during the fixation of N2 by nodule bacteria. Therefore, roots acquire N in small portions, but more continuously and mainly unidirectionally. This leads to the continuous accumulation of N in roots and its depletion in the rhizosphere. Some of the N is involved in the synthesis of amino acids and proteins in roots, whereas another part is translocated to the shoots for further utilization. This indicates that, over long periods, plants acquire increasing amounts of N, which had already passed through a microbial cycle(s) and was initially stored in the SOM. At an ecosystem level, plants and microorganisms obtain the N as required (Kaye & Hart, 1997).