of gross mineralization, immobilisation and nitrification is also a key for understanding the competition ..... control (Hamilton and Frank 2001). This may apply as ...
The International Fertilizer ISBN-10: 0853102031
Society,
Proceedings
n°566,
December
2005.
SOIL MICROBIAL BIOMASS: ITS ROLE IN NITROGEN CYCLING AND EFFICIENCY Sylvie Recous INRA, Unité d’Agronomie, rue F. Christ, 02007 Laon cedex, France ABSTRACT Understanding the factors that govern microbial activities in soils is important, as the heterotrophic soil microbial biomass is driving the C and N cycling, and the net availability of N for plant uptake or losses. The processes by which C and N interact during decomposition of organic matter in soil, and the mineralization-immobilisation turnover are well known but still difficult to predict, due to the complex interactions between soil microorganisms and their substrates. The 15N isotope dilution techniques that allow quantifying accurately and simultaneously rates of N transformations, help understanding the effects of soil, crop and management conditions on microbial activities. The quantification of the relative importance of gross mineralization, immobilisation and nitrification is also a key for understanding the competition between processes and the susceptibility of systems to lose or retain nitrogen.
INTRODUCTION There has been considerable research over the last thirty years into the factors and conditions determining dynamics of nitrogen in soils. The main practical application of this research was the development of methods for predicting the soil nitrogen supply (net mineralization) and the fate of added fertiliser-N in order to improve fertiliser recommendations. Soil microbes, despite representing a few percent of the total soil organic C and N, have a crucial role in C and N cycling, due to their fast turnover. They affect the availability of soil N for uptake or loss mainly through the concurrent processes of mineralisation and immobilisation, and the balance between ammonium and nitrate forms through the nitrification process. The size and activity of the soil biomass is related to the quality of soil organic matter and to other physical, chemical and environmental parameters. Understanding their role is therefore important from both the management and ecological perspectives, particularly because management practices imposed on agricultural systems often disturb soils. Still there is a lack of understanding of the links between soil microbial properties (structure, metabolism, activity) and C and N fluxes, and a lot of uncertainty in the prediction of nutrient availability in soils. That explains the considerable research effort that is developing in various agro-ecosystems, particularly in combination with isotope studies.
1. MINERALISATION-IMMOBILISATION TURNOVER IN SOIL Inorganic N is made available by the mineralisation of organic N to ammonium (NH4+) and subsequent nitrification (mainly autotrophic) to nitrate (NO3-). The availability of ammonium and nitrate in soils results from the competition between several opposing soil processes:
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(i) the gross mineralisation corresponds to the oxidation of SOM by endocellular and exocellular enzymes from a wide range of non-specific micro-organisms and produces the release of NH4+ into the soil solution during the decomposition of soil organic matter (SOM); it is determined by SOM content and soil properties such as clay and CaCO3 content, pH. Across a large range of soil and climatic conditions gross mineralisation is closely related to total organic C and biomass C (Booth et al., 2005). (ii) the gross immobilisation corresponds to the assimilation of inorganic nitrogen by soil heterotrophic micro-organisms, the growth and activity of which depend on the availability of organic C. Gross immobilisation affects both the ammonium and nitrate forms, and is mainly driven by the availability of easily decomposable organic C. Rate of immobilisation can change quite rapidly according to C inputs and their dynamics of decomposition. Mineralisation and immobilisation of N occur simultaneously and therefore N is continually transferred within the soil from organic to inorganic forms and vice versa through the Mineralisation-Immobilisation Turnover (MIT). That causes the MineralisationImmobilisation turnover of N (M.I.T.) in soil to be linked to the cycling of C. (iii)The nitrification of NH4+ to NO3- by the nitrifying micro-flora. Autotrophic nitrifiers gain energy by converting NH4+ to NO3-. Nitrification rate is quite variable and in agricultural soils often highly dependent on soil pH, although this relationships is a matter of debate, and very sensitive to temperature. High rates of nitrification are also found in some acidic forest soils, probably as a consequence of the adaptations of nitrifying microorganisms and of their localisation in specific soil sites. Therefore the three processes do not respond to the same soil factors. They also have different sensitivity to temperature and soil water content (Hoyle et al., 2005). C and N dynamics are closely linked and this link is the key for understanding both the short and the long-term evolution of N in soils. Indeed most of the soil microorganisms are usually limited by the supply of easily decomposable carbon in soil, as they are heterotrophic i.e. they gain their energy from the oxidation of organic substrates and assimilate also C for growth. The C assimilation rate depends on the rate of decomposition of plant material and the assimilation yield of the decomposed C by the microorganisms. During the decomposition simultaneous assimilation of C and N occurred. CO2 C N mineralisation
Crop residues assimilation
recycling
humification
Microbial biomass
Soil organic matter
assimilation humification
mineralisation
immobilisation
Soil mineral N
Figure 1: Main processes affecting C and N cycles during the decomposition of organic matters in soil by soil heterotrophic microflora.
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Heterotrophic bacteria and fungi have high N requirements as their C:N ratio are ranging from 4:1 to 12:1. The carbon flow and the C:N ratio of the decomposers then determine the N assimilation requirements (Figure 1). As the heterotrophs respire about 50% of their C uptake, the decomposition of humified organic matter leads to the net release of inorganic N in soil. When organic matter is added, the decomposition leads either to net release or to the temporary net immobilisation of inorganic N in soil. (Figure 2) The dynamics as well as the net amounts of N immobilised vary greatly according to the nature of plant residues (chemical characteristics) and nitrogen content of the various organic pools. CO2
CO2
60 g C
60 g C
Straw (C:N = 100) 100 g C, 1 g N
Microbial biomass (C:N =8) 40 g C, 5g N
Net immobilisation Soil mineral N -4gN
Soil O.M. (C:N = 11) 100 g C, 11 g N
Microbial biomass (C:N =8) 40 g C, 5g N
Net mineralisation Soil mineral N +6gN
Figure 2: Examples showing the relationships C:N ratio of organic pools decomposing C:N ratio of the soil biomass and net fluxes of mineral N in soils. The calculation was done assuming an assimilation yield of carbon of 0.4, a similar ratio for the soil biomass decomposing straw and humified organic matter, and an initial C:N ratio of the organic pools of 100 (straw) and 11 (organic matter).
For example Mary et al. (1996) reported a net mineralisation of +15 mg N per gram of added C for wheat leaves, and a net immobilisation of -28 mg N per gram of added C for wheat straw and -72 for root mucilage. Indeed there is a general agreement on the fact that the threshold between net release of N and net immobilisation of mineral N in soil occurs with a residue C:N ratio of about 25, limit above which the microbial N demand during decomposition is no more fulfilled by the N supply from the crop residue. Dynamics of net accumulation of N varies with time and consequently the net effect of incorporating a C source on soil N depends mostly on the time scale on which the N effect is considered. On the short-term it appears that only a few residues lead to the rapid net release of N while most of them provoke a phase of net immobilisation, followed by a phase of net mineralisation, the magnitude and the duration of which depends of the overall N content of soil + residue and the biochemical residue quality itself (Trinsoutrot et al., 2000). The C:N ratio of soil micro-organisms is smaller than those of most plant residues and therefore the external source of N can be rapidly exhausted. The rate of decomposition of the residues is therefore often limited by the availability of mineral N even in situation with frequent addition of mineral N (Mary et al., 1996). For example, one can calculate that 8 tons per hectare of wheat straw incorporated into the top 10 cm of soil would require the immobilisation of about 130 kg N /ha to be decomposed. Indeed this amount of N will not usually be available in the soil layer concerned, and the decomposition would slow down. 3
In turn, this may result in the accumulation of undecomposed debris, creating a potential for N immobilisation when N will become available (e.g. after fertiliser application). The availability of nitrogen in soil controls the decomposition and dynamics of C in soil on both the short- and long-terms. This fact has been established for a long time for various types of plant residues (Fog, 1988). On the short term, little N availability will restrict the growth of heterotrophs. On the longer term, N availability also influences the decay process because high N availability is known to inhibit the synthesis of ligninolytic enzyme systems. The complex interactions between N and type of residues, type of decomposers and the chemical reactions during humification have been described (Fog, 1988) For plant residue of high C:N ratio, as mature straw, it has been demonstrated that the shortage of N during decomposition not only reduces initial rates of decomposition of OM but also modifies the relationships between decomposed C and immobilised N. When N was abundant, an immobilisation ratio of 32 mg N immobilised per g of added straw-C was calculated, and this value was similar to the immobilisation ratio obtained in optimal conditions of decomposition (e.g. Henriksen and Breland, 1999). When N was limiting, the immobilisation ratio decreased accordingly. Several hypotheses may explain that changes, such as a change in microbial succession, the adaptation of internal N content of fungi, the modification of energy allocated to growth or to maintenance, or an increase in the rate of biomass recycling. This has been clearly demonstrated under controlled conditions but also in the field (Mary et al., 1996). Like the N produced by mineralisation of native soil organic matter, N added as mineral fertilizer is involved in this mineralisation-immobilisation turnover. The immobilisation rate of fertilizer N is determined by the immobilisation capacity of soil which depends on its C availability. The main sources of C in cropped soils are root systems through root litter, rhizodeposition and exudation, plus other crop residues that may be returned to the soil. The amount of N (either from soil or from fertilizer) which is immobilised due to heterotrophic microbial activity is therefore determined both by the availability of C and N in soil. Any extra N (added by fertilizer) can contribute to the decomposition of residues in soil. Therefore in field conditions the dynamics of organic matter is often driven by the availability of N at the site of decomposition. This is the case for situations with low soil N content at time of residues incorporation and/or of uneven spatial distribution of crop residues into the soil. Indeed the “new” organic matter entering the soil (through the root systems and the returning crop residues) is always patchily distributed throughout the soil in both space and time, and its decomposition creates temporarily C-rich patches for microorganims, that may be very often N-limited for microbial growth. This situation is aggravated in reduced or no-tilled systems where mulch of residues are left onto the soil surface. In that case, the spatial separation of residue-C and soil N is furthered by the limited contact of decomposing residues with soil. Coppens et al. (2006) observed that the presence of rape residues as a mulch over the soil surface compared to incorporated residues, increased both the water content of the soil layer underneath and the subsequent soil N mineralisation and decreased the N immobilisation, leading to higher net nitrate accumulation and transport down the soil profile. It is therefore complex to predict the net availability of inorganic N in soil as it is the result of dynamic and opposite processes of mineralisation and immobilisation, the latter under the control of C cycle and decomposers and linked to the overall residue+soil N availability.
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2. QUANTIFICATION OF N BIOTRANSFORMATIONS Owing to the complexity of the various N fluxes acting in opposite direction (release or consumption of N) 15N tracing has been central to understand the mechanisms involved and it is still the sole option to quantify the gross N biotransformation. Several methods involving label 15N have been developed. The widely used approach is that consisting in adding homogeneously 15N-labelled residues. Labelling the added organic source allows to trace the fate of the added N in the various soil pools and to measure recovery of the added 15N in plant. All observed a rather low availability of the added 15N measured in a subsequent crop (7-26% of the added 15N), indicative of a large immobilisation and stabilisation in soil. Alternatively or in parallel, the soil inorganic N pool can be labelled with 15N. That allows quantifying over time the net immobilisation of soil N during the decomposition process. This approach shows that soil N contributes much to the microbial immobilisation process, to an extent that can be closely related to the residue-N content itself (Trinsoutrot et al., 2000). In such experiments, the observed increase in the 15N enrichment of residues -initially unlabelled- during decomposition demonstrated that the decomposers are growing on the particulate matter itself while their N requirements are fulfilled from the surrounding labelled soil N (Cheschire et al., 1999). Research dealing with the quantification of "gross N fluxes" received much attention during the last decade. Knowledge of the actual rates of these processes in soil can be very useful in understanding how soil and crop management affects N turnover, or to evaluate some of the concepts introduced in C-N biotransformation models, as most of them describe first the gross N transformations, from which the net mineralisation is calculated. Only 15Nisotope tracing allows calculating separately the two processes. Based on the "dilution principle" gross N mineralisation is calculated, after labelling homogeneously with 15N the soil NH4+ pool, from the decrease in 15N enrichment and the change in the size of the soil ammonium pool as micro-organisms mineralise native soil organic matter-14N to 14NH4+. Nitrification and immobilisation can be calculated from the enrichment in 15N of the nitrate or organic N pool, or from the consumption of the ammonium (Murphy et al., 2003) The gross flux method differs fundamentally from the previous ones, because it aims at tracing the whole soil mineral pool and not only the fate of the added label N. Therefore the method involved conditions (homogeneity of labelling, equilibrium between added and native N, etc.) that are difficult to obtain. Consequently, much research has been already done to look at the best method to apply the label (e.g. spray vs. injection), to obtain homogeneity in the distribution of the label into the soil cores, to determine the optimal duration for incubations (Murphy et al., 1998). Despite these difficulties, the gross fluxes approach yielded useful information on estimates of actual gross fluxes under grasslands (Hatch et al., 2000; Schimel, 1986), forests (Hart et al., 1994; Pulleman et al., 1999), the changes in gross mineralisation and immobilisation during decomposition of crop residues and organic wastes (Recous et al., 1999; Shindo and Nishio, 2005). Alternative use of the gross flux technique has been developed also to study the effect of factors on the N processes. In this later case, gross fluxes technique is used in controlled conditions to assess the effect of various factors on potential gross mineralisation, immobilisation or nitrification (e.g. effect of soil disturbance, soil re-moistening, soil temperature, type of plant cover). Particularly in forest ecosystems, studies of soils below different tree species show that deciduous species tend to promote nitrification as compared to coniferous species (Augusto and Ranger, 2001). In herbaceous species, it has been shown that plants may positively or negatively influence nitrification, but no simple general mechanism has been proposed up to now, to explain this control (Hamilton and Frank 2001). This may apply as well to arable situations.
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The gross flux approach gives information on instantaneous rates of mineralisation, immobilisation and nitrification. In that respect it is a very useful tool to analyze competition between them and to assess relationships with other processes (e.g. C dynamics). Close relationships are found between gross mineralisation or gross immobilisation and C respiration or microbial C as both are related to soil organic C (e.g. Recous et al., 1999). Assembling a large data set on soil characteristics and gross rates from 100 studies conducted in forest, grassland and agricultural systems, Booth et al. (2005) confirmed that N mineralisation were highest in grasslands, intermediate in woodlands and lowest in agricultural system; ammonium assimilation (immobilisation) had the same ranking while nitrification did not differ significantly among the vegetation types confirming little relationships between nitrification and soil organic pools. In agricultural soils, the large variation observed in nitrification rates - compared to mineralisation - can make either mineralisation (production of NH4+) or nitrification (consumption of NH4+) being the limiting step of nitrate dynamics and therefore nitrification influence much the overall nitrate availability and potential N losses from the soil-plant system as discussed later.
3. EFFECTS OF CROP COVER AND MANAGEMENT ON N FLUXES How is MIT influenced by crop type and management? The first way may be through the crop root system. There have been many attempts to quantify the possible direct effects (e.g. C exudation) and indirect effects (e.g. depletion of mineral N by absorption) of plant growth on soil heterotrophic microflora and to understand how their opposite and concomitant effects drives actually the gross immobilisation and mineralisation and determine the resulting net mineralisation. The difficulties of using the isotope 15N method at the mm-scale in the root rhizosphere of a living plant without disturbing the processes have made the challenge quite impossible until now. Mary and Recous (1994) simulated the order of magnitude of gross mineralisation and immobilisation fluxes in a continuous wheat rotation with the usual amount of organic restitution in Northern Europe. Using data from the literature, obtained under laboratory conditions, they estimated the potential N immobilisation associated to the decomposition of wheat straw, root litter and root exudates (mucilage) to be about 300 kg/ha over the year. In this situation, net mineralisation, gross immobilisation and gross mineralisation were in the ratio 1:2:3. Tlustos et al. (1998) found that permanent grassland soil exhibited MIT turnover rates 30 times higher than those in arable soil, although net N mineralisation rates were similar between systems. Studies using 15N tracing of fertilizer on grasslands also showed that the fertilizer –N disappeared very quickly from soil due to the intensity of microbial immobilisation, and was recovered later by the plant, in significant proportion, thanks to the fast microbial turnover (i.e. high rate of gross mineralisation). Therefore the type of crop and the conditions of growth of a crop - that affect the nature and amount of rhizodeposits and the associated rhizosphere microflora- can alter significantly the soil N supply, either by modifying the gross mineralisation or the gross immobilisation or both, even if this is difficult to quantify at the rhizosphere scale. The second way by which a crop interacts with the soil N cycle is through the above-ground residues that return to soil by senescence or after harvesting. Organic residue input influence microbial population density, microbial diversity and immobilisation of nitrogen (N) by changing the readily available carbon, which is essential for maintaining microbial growth and activity – as explained earlier. Using the 15N dilution technique associated with the monitoring of C decomposition in laboratory conditions, Watkins and Barraglough (1996) and
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Shindo and Nishio (2005) found that incorporation of oilseed rape stems or wheat straw were immediately followed by increase in both gross mineralisation and gross immobilisation and was associated to a rapid increase of microbial biomass. It indicates not only the expected immobilisation effect of decomposing high C:N substrate, but also a priming effect on the (gross) mineralisation of soil organic matter. Using field values and a model to simulate N fluxes over one-year long study, Garnier et al. (2003) found that the cumulative gross N fluxes associated to the decomposition of 8 tons of wheat straw was 743 kg N ha -1 for gross mineralisation, 580 kg N ha-1 for gross immobilisation, leading to a net mineralisation of 163 kg N ha-1. The changes in gross N fluxes associated to the decomposition of straw were completed after one year in the field. The combined use of 15N dilution technique and of the monitoring of decomposition (CO2) allow to enlighten the effects of the biochemical composition of organic wastes on the dynamics of N (Flavel et al. 2005; Morvan, 2005 ). These studies reveal that the magnitude of gross N fluxes in soil is very much larger than the net N mineralisation that determines ‘theoretically’ the availability of mineral nitrogen in a soil. Most of the potential interactions between release of C and N, uptake of N, microbial and micro-fauna growth and death, and the associated gross mineralisation and gross immobilisation processes concern a small volume of soil, due to the mm scale of the rhizospheric processes and the patchy localisation of decomposing organic matters. Nevertheless, the high intensity of these processes can lead to an overall effect at integrated soil layer scale. So different crops growing on the same soil could have different N uptake capacity only because they can affect the equilibrium between gross mineralisation and gross immobilisation, therefore changing the net mineralisation of N. Differences in soil N uptake capacity between crop species may be explained by the possibility of plants to alter the MIT. A higher specific N uptake capacity of roots (high affinity system) could enable a crop species to reduce the residence time of mineral N in soil and then to decrease its probability to be assimilated by the rhizosphere microflora; a specific C root exudate compound could stimulate either gross mineralisation or gross immobilisation. Thereofore the concept of “soil N supply” to a crop can no longer considered by itself i.e. as a function of soil characteristics and climatic conditions only, but should be considered also as dependent on the interactions between crop and soil processes. In order to understand the relationships between plant species and soil functioning, much research currently investigates the effects of plant species and/or cropping history on microbial community (e.g. Böhme et al., 2005; Hackl et al., 2005; Innes et al., 2004, Zaman et al., 2004). They all show changes in microbial community structures or microbial metabolism although the mechanisms for such changes and the relationships with microbial activities and fluxes are still difficult to make (Lupwayi et al., 2004).
4. COMPETITION FOR NITROGEN BETWEEN PROCESSES The use of 15N isotopic tracer techniques has enabled greater resolution and understanding of the processes that control N supply for plant uptake and N losses. Microbial mineralisation and nitrification are generally thought to be the rate-limiting steps in the N cycle and it has thus been assumed that microorganisms are able to acquire inorganic N before plants. It is difficult to assess direct competition between plants and microorganismes for soil N or competition between the different microbial processes, because there are multiple loops and pathways through which N cycles at variable and in varying amounts between different pools. As pointed out already by Jansson (1958) the microbial immobilisation of N is a major process in the soil. At the scale of the cropping system, the mineralization-immobilisation
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balance drives the dynamics of inorganic N in soil; on an annual crop time-step, gross immobilisation, hidden by a dominating mineralisation process, determines part of the fertilizer-N uptake efficiency. Competition between plants and microorganims is believed to be intense and therefore considerable attention has been paid to analyse and understand the outputs of plant-heterotrophs competition, in order to better manage nitrogen (Kaye and Hart, 1997). For example labelling the NH4+ and NO3- pools of a grassland soil with 15N revealed that, even though the NH4+ pool was very dynamic and had a fast turnover, of about 1 day. It translated into a fast disappearance of the labelled added N, a simultaneous rapid labelling of the organic pool indicative of large microbial immobilisation, and consequently a low recovery of the added N into the plant. On the longer term, the recycling of the soil labelled biomass turns into a release of the immobilised N and a subsequent re-use by the crop. The rapid turnover of microbial biomass gives the roots an opportunity to capture the released N through microbial cell lysis, making the plants better competitors on the longer term (Hodge et al. 2000). Field experiments also conducted with labelled N often showed lower recovery of the labelled NH4+ than NO3- in the plant. This lower recovery was attributed to a higher immobilisation in the case of NH4 than for NO3 fertilizers (Powlson et al., 1986, Recous et al., 1992) and this was due to preferential assimilation of NH4+ to NO3+ by soil heterotrophic microorganisms. It was shown that when nitrate and ammonium are available simultaneously as source of nitrogen for pure cultures of bacteria isolated from soils, ammonium suppresses the microbial uptake of nitrate (Recous et al. 1990; Rice and Tiedje, 1989); when nitrate was the sole source of nitrogen, it was used to the same extent as the ammonium form. It means that nitrate is potentially less subjected to immobilisation than ammonium and potentially more available in soil, particularly for plant uptake. However, as pointed out by Hodge et al. (2000), due to the spatial differences in nitrogen availability, roots and microbial distributions, it is not possible to discuss plant-microorganisms competition without taking into account this spatiotemporal context. It is particularly true for the comparison of ammonium and nitrate availability to plant uptake, ammonium being less mobile compared to nitrate and therefore not available at the same site than nitrate. The same concept applies to the competition for ammonium between immobilisation and nitrification. Numerous results in controlled conditions showed the fast depletion of soil ammonium pool after a C-substrate was added, without any nitrate production. Actually, in soils, sites showing either net immobilisation or nitrification and net mineralisation exist, as a result of the heterogeneous distribution of organic matter, water, physical and chemical soil properties. The same concepts and techniques have been applied at a larger scale to obtain measurements of potential N loss. The relative dominance of the pathways of ammonium consumption via nitrification or immobilisation of N by the microbial biomass can be expressed in the ratio Nitrification/Immobilisation (N/I). Tietema and Wessel (1992) suggested that forest soils with a high N/I ratio have a greater potential to lose N from the system via leaching or denitrification than those with a low N/I. Stockdale et al. (2002) used also this ratio to show that in grasslands and arable fields the N/I ratio was able to discriminate well the various systems for their susceptibility to losses by leaching. However it was not possible to well explain changes in individual fluxes (e.g. the effects of agricultural practices on nitrification rates) and further research to understand factors that affect processes, particularly nitrification is still necessary.
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5. CONCLUSION The central role of the MIT in the dynamics of C and N in soil and the theoretical basis for using isotope dilution techniques were developed about 50 years ago, and much work has been undergone to study the dynamics of soil and fertiliser-N and the net availability of N since that time. Despite methodological limits, the ‘gross flux’ approach has proved being powerful for improving understanding of the relationships between C, N dynamics and soil heterotrophic microflora. This is due the sensitivity of the method and its ability to quantify rates of microbial processes at a time-scale that allow linking changes in the size of some C pools (e.g. soluble C, microbial C) with N fluxes. However a better understanding of the factors that affect nitrifying microorganisms and their activity is still required to predict the availability of the mineral N forms in soils and consequently the potential of systems to lose N under various forms. The current research put emphasis on assessing the effects of crop management and agricultural practices on soil microorganisms or some of their components – community structure, metabolism parameters, microbial activities- in order to understand resistance or resilience of cropping systems to changes There stands the challenge of linking those characteristics of soil microflora with microbial functions and nutrient dynamics in soil.
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