Mineralisation and sorption of dissolved organic nitrogen compounds in litter and soil from sugarcane fields
Graphical abstract
Introduction
In the southeast region of Brazil, the burning and manual harvesting of sugarcane (Saccharum spp.) has been extensively replaced by mechanical harvesting, without burning, owing to environmental, economic, social, and human health concerns (Galdos et al., 2013). This modern harvest system promotes the deposition of leaves and other debris on the soil surface, which can result in an annual input of between 10 and 20 Mg ha−1 (dry weight) of crop residue in sugarcane fields (Leal et al., 2013). However, along with crushed bagasse, sugarcane litter can also been used in the cogeneration of heat and electricity in mills (Leal et al., 2013), and the ever-growing possibility of second generation bioethanol production from the enzymatic hydrolysis of lignocellulosic materials, including sugarcane litter, has also raised important discussions regarding the removal of the residue from sugarcane fields (Cantarella et al., 2013, Leal et al., 2013, Sordi and Manechini, 2013). The main benefits of litter deposition are related to increases in soil microbial activity, soil moisture content, soil C storage, nutrient cycling, stability of soil temperature, and erosion control (Dourado-Neto et al., 1999, Sparovek and Schnug, 2001, Cerri et al., 2011, Franco et al., 2013, Azevedo et al., 2014), whereas the disadvantages include increased incidence of some plant pests (as the litter provides a more conducive habitat for pathogen persistence; Dinardo-Miranda and Fracasso, 2013) and ammonia volatilisation from urea fertiliser (higher urease activity is reported in plant residues than in soil; Barreto and Westerman, 1989). In addition, the influence of litter deposition on the supply of N to sugarcane is another subject that has attracted interest from both scientists and farmers, owing to its role in proper N fertiliser management (Fortes et al., 2011, Fortes et al., 2012, Fortes et al., 2013, Trivelin et al., 2013). It is generally assumed that plant litter and humus are the two most important sources of dissolved organic matter (DOM) in soils, and its release into solution occurs through physicochemical decomposition and leaching from litter and formation of humic substances (Kalbitz et al., 2000). However, despite the low net N mineralisation of sugarcane residue (Fortes et al., 2012), studies characterizing organic N fractions contained in the litter layer that can be mineralised in the short term, to our knowledge, are scarce.
The last 25 years has seen a progressive shift in our understanding of terrestrial N cycling. In particular, and in contrast to the traditional paradigm of N cycling, it has been shown that a wide range of low molecular weight dissolved organic N (DON) compounds can be directly taken up by plant roots, along with inorganic forms of N (NH4+, NO2−, and NO3−; Barak et al., 1990, Schimel and Bennett, 2004, Jones et al., 2005, Nannipieri and Paul, 2009, Kuzyakov and Xu, 2013). Although mineralisation and immobilisation processes drive nutrient availability to plants in the classical N cycle model, the depolymerisation of organic N compounds plays a key role in the N cycling in the new conceptual paradigm (Schimel and Bennett, 2004). Depolymerisation occurs through extracellular enzymes that are produced by microbes and are capable of cleaving polymers to smaller polymers or monomers. As a consequence, these low molecular weight DON compounds (e.g., amino acids and oligopeptides) can be rapidly mineralised and nitrified, or even taken up by plants in an intact form (Schimel and Bennett, 2004, Jones et al., 2005, Hill et al., 2011). For this reason, the contribution of organic N from litter to the N supply of growing sugarcane might have been underestimated and should be investigated more fully (Brackin et al., 2015).
The net N mineralisation of low molecular weight DON compounds by microbes also has an important effect on the bioavailability of inorganic N forms. Rapid cycling of amino acids and peptides has been extensively observed in temperate soils, using 14C tracers to measure C mineralisation (Jones and Kielland, 2002, Jones et al., 2004, Jones et al., 2009, Farrell et al., 2011, Glanville et al., 2012, Wilkinson et al., 2014). The rapid mineralisation of oligopeptides is explained by its intact uptake by soil microbes, including mycorrhizas, especially in N-limited ecosystems (Farrell et al., 2011, Hill et al., 2012). However, the mineralisation of urea and protein, a low and high molecular weight DON compound, respectively, is still unclear. Although the behaviour of urea as an N fertiliser has been broadly studied and recognized (Bremner, 1995), measurements of its turnover are restricted to temperate soils, where high rates of urea catabolism have been described (Nielsen et al., 1998, Glanville et al., 2012). In contrast, Jones and Kielland (2012) reported low protein mineralisation rates in a taiga forest soil, owing to the wide range of extracellular enzymes required for its cleavage into monomers. Alongside the variable mineralisation of different DON compounds, the uptake of DON by microbes from the sugarcane litter may primarily provide them with C to fuel respiration, thus resulting in lower C use efficiency (CUE) and consequent higher C mineralisation, since the crop residue has a greater C-to-N ratio than the underlying soil (Sinsabaugh et al., 2013). In addition, distinct microbial communities between litter and soil can also affect the C and N turnover (Creamer et al., 2015).
Alongside mineralisation, sorption to the solid phase plays an important role in regulating the dynamics of DON in soil. There is ample evidence that sorption of DON can stabilise and promote the accumulation of organic matter in subsoil horizons, although it has also been proposed that biofilms covering mineral surfaces may counteract this to some extent (Guggenberger and Kaiser, 2003, Marschner and Kalbitz, 2003). Most amino acids and peptides are weakly sorbed to the soil solid phase, thus exhibiting relatively high bioavailability (Amelung et al., 2002, Roberts et al., 2007, Ge et al., 2012). On the other hand, the sorption of urea is variable and occurs through hydrogen bonding mainly from amino hydrogens, whereas protein is suggested to readily sorb to the colloid solid phase (Mitsui et al., 1960, Said, 1972, Baron et al., 1997). Meanwhile, the sorption affinity of DON compounds in the litter layer is entirely unknown. However, when the sorption equilibrium between the solid and liquid phase is changed through DON depletion, part of the sorbed fraction may be released back into solution, in order to restore the previous equilibrium. Thus, if the litter layer has a significant sorption capacity, its presence may also mitigate losses of DON which would otherwise be leached down the soil profile.
On the basis of the recently proposed model of the N cycle, we believe that understanding the dynamics of DON compounds in the litter and soil of sugarcane fields is essential to increasing the sustainability of sugarcane production in Brazil, as well as in other countries. Research regarding this topic could also close gaps in our current knowledge by providing additional information about the role of litter in terrestrial N cycling. Accordingly, the aim of the present study was to evaluate the reactions (C mineralisation and sorption) of 14C-labelled DON compounds (amino acids, peptides, urea, and protein) in litter and soil from two sugarcane fields located in Brazil. We hypothesised (i) that the C mineralisation of amino acids, peptides, and urea by litter and soil microbes would be more rapid than the mineralisation of protein, (ii) that DON compounds would be taken up more slowly in soil than in litter, and (iii) that the sorption affinity of protein would be higher than that of the other DON compounds.
Section snippets
Site characteristics
Litter and soil samples were collected from two sugarcane N rate-response experiments located in São Paulo, Brazil. At both experimental sites, sugarcane is planted ca. every six years and is harvested annually. Before crop replanting, soil tillage (ploughing, harrowing, and furrow opening), lime and gypsum application, and the sowing of atmospheric N2-fixing legume plants are usually performed.
Site 1 was located in Novo Horizonte (21°32′S, 49°20′W), where the sandy loam soil (825 g kg−1 sand,
Chemistry of water and potassium sulphate extracts
More NH4+-N was detected in the water and K2SO4 extracts of the litter than in extracts of the soil at Site 1 (Table 2). However, the NO3−-N content was higher in the soil at both experimental sites, regardless of the extractant (water or K2SO4), as was also the case for the TIN. Much higher DOC, DON, DOC-to-DON ratio, and phenolic values were observed in the water extracts of litter than in the water extracts of soil at Site 1 (Table 2). Similar differences were also detected in the K2SO4
Litter and soil characteristics
The NH4+-N content found in the litter and soil at both sites was extremely low (<1 mg dm−3), indicating high consumption of this inorganic N fraction, most likely due to NH4+ immobilisation in the high C-to-N ratio litter, and also due to nitrification in the soil. The contrasting C-to-N ratio of the litter, compared to the soil (Table 1), supports this hypothesis (Mary et al., 1996). In contrast, the much higher NO3−-N content compared to NH4+-N detected in the soil may be explained by high
Acknowledgments
The first author (EM) was supported by a scholarship from the São Paulo Research Foundation (FAPESP; Process n. 2013/3866-1), and this work was funded by the UK Natural Environment Research Council (NERC). We would like to thank Beatriz N. Boschiero and Rafael Otto for their assistance in collecting litter and soil samples, as well as Fernando D. Andreote and Thiago Gumiere for their advice regarding statistical analysis of the microbial community structure.
References (84)
- et al.
Fast turnover of low molecular weight components of the dissolved organic carbon pool of temperate grassland field
Soil Biol. Biochem.
(2007) - et al.
High throughput phospholipid fatty acid analysis of soils
Appl. Soil Ecol.
(2012) - et al.
Factors affecting soil microbial community strucuture in tomato cropping systems
Soil Biol. Biochem.
(2010) - et al.
Sites of microbial assimilation, and turnover of soluble and particulate 14C-labelled substrates decomposing in a clay soil
Soil Biol. Biochem.
(1998) - et al.
Microbial community structure mediates response of soil C decomposition to litter addition and warming
Soil Biol. Biochem.
(2015) - et al.
Long-term decomposition of sugarcane harvest residues in São Paulo State, Brazil
Biomass Bioenerg.
(2012) - et al.
Microbial biomass measured as total lipid phosphate in soils of different organic content
J. Microbiol. Methods
(1991) - et al.
Use and misuse of PLFA measurements in soils
Soil Biol. Biochem.
(2011) - et al.
Trends in global warming and human health impacts related to Brazilian sugarcane ethanol production considering black carbon emissions
Appl. Energ.
(2013) - et al.
Mineralization of low molecular weight carbon substrates in soil solution under laboratory and field conditions
Soil Biol. Biochem.
(2012)
Combined use of empirical data and mathematical modelling to better estimate the microbial turnover of isotopically labelled carbon substrates in soil
Soil Biol. Biochem.
Dissolved organic matter in soil: challenging the paradigm of sorptive preservation
Geoderma
Bigger may be better in soil N cycling: does rapid acquisition of small l-peptides by soil microbes dominate fluxes of protein-derived N in soil?
Soil Biol. Biochem.
Ninhydrin-reactive nitrogen measurements of microbial biomass in 0.5 M K2SO4 soil extracts
Soil Biol. Biochem.
Soil amino acid turnover dominates the nitrogen flux in permafrost-dominated taiga forest soils
Soil Biol. Biochem.
Amino acid, peptide and protein mineralization dynamics in a taiga forest soil
Soil Biol. Biochem.
Experimental evaluation of methods to quantify dissolved organic nitrogen (DON) and dissolved organic carbon (DOC) in soil
Soil Biol. Biochem.
Simple method to enable the high resolution determination of total free amino acids in soil solutions soil extracts
Soil Biol. Biochem.
Role of dissolved organic nitrogen (DON) in soil N cycling in grassland soils
Soil Biol. Biochem.
Dissolved organic nitrogen uptake by plants – an important N uptake pathway?
Soil Biol. Biochem.
Glucose uptake by maize roots and its transformation in the rhizosphere
Soil Biol. Biochem.
Sugarcane straw availability, quality, recovery and energy use: a literature review
Biomass & Bioenergy
Controls of bioavailability and biodegradability of dissolved organic matter in soils
Geoderma
A rapid, simple spectrophotometric method for simultaneous detection of nitrate and nitrite. Nitric oxide
Biol. Chem.
The chemical and functional characterization of soil N and its biotic components
Soil Biol. Biochem.
Methodology for studying fluxes of soil mineral-N in situ
Soil Biol. Biochem.
Free amino sugar reactions in soil in relation to soil carbon and nitrogen cycling
Soil Biol. Biochem.
Loss of low molecular weight dissolved organic carbon (DOC) and nitrogen (DON) in H2O and 0.5 M K2SO4 soil extracts
Soil Biol. Biochem.
14C-labelled glucose turnover in New Zealand soils
Soil Biol. Biochem.
Considering fungal:bacterial dominance is soils: methods, controls, and ecosystem implications
Soil Biol. Biochem.
Rapid microbial uptake and mineralization of amino acids and peptides along a grassland productivity gradient
Soil Biol. Biochem.
Phospholipid fatty acid profiles in selected members of soil microbial communities
Chemosphere
Fate of microbial residues in sandy soils of the South African Highveld as influenced by prolonged arable cropping
Eur. J. Soil Sci.
The role of dissolved organic nitrogen in phytoplankton nutrition, cell biology and ecology
Phycologia
Early changes in arbuscular mycorrhizal development in sugarcane under two harvest management systems
Braz. J. Microbiol.
Mineralization of amino acids and evidence of direct assimilation of organic nitrogen
Soil Sci. Soc. Am. J.
Protein adsorption on soil mineral surfaces
Soil urease activity in winter wheat residue management systems
Soil Sci. Soc. Am. J.
Nitrogen fluxes at the root-soil interface show a mismatch of nitrogen fertilizer supply and sugarcane root uptake capacity
Sci. Rep.
Recent research on problems in the use of urea as a nitrogen fertilizer
Fertil. Res.
Nitrate sorption in the profile of an acid soil
Plant and Soil
How much sugarcane trash should be left on the soil?
Sci. Agric.
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