Elsevier

Soil Biology and Biochemistry

Volume 103, December 2016, Pages 522-532
Soil Biology and Biochemistry

Mineralisation and sorption of dissolved organic nitrogen compounds in litter and soil from sugarcane fields

https://doi.org/10.1016/j.soilbio.2016.10.004Get rights and content

Highlights

  • Sugarcane litter and soil had different microbial community structures.

  • Mineral N content was higher in soil, and DON content was higher in litter.

  • Amino acids, peptides, and urea were weakly sorbed and rapidly mineralised.

  • Protein exhibited the slowest mineralisation and the highest sorption affinity.

Abstract

Dissolved organic nitrogen (DON) represents an important soluble nutrient pool in soil, however, little is known about the dynamics of DON in the litter and topsoil of Brazilian sugarcane (Saccharum spp.) fields, particularly those that are harvested mechanically, without burning. Therefore, the aim of this study was to determine the microbial mineralisation and sorption affinity of DON compounds in litter and soil from the litter-soil transition zone of two sugarcane plantations located in southeastern Brazil. We directly measured the C mineralisation of 14C-labelled amino acids (mix of 17 amino acids), peptides (l-dialanine and l-trialanine), urea, and protein (isolated from tobacco leaves) by capturing 14CO2 evolved from the litter and soil over 168 h. A sorption assay was performed using the same treatments. We found differences in the organic and mineral N pools of the litter and soil, as well as in microbial community composition. Except for protein in the soil, the DON compounds were taken up rapidly by microbes. However, the C use efficiency was higher for the amino acid mix than for the peptides and urea, indicating more rapid post-uptake catabolism (with subsequent mineralisation as 14CO2) of both compounds. In addition, protein had the highest sorption affinity, especially in soil, and the weak sorption affinity of the amino acids, peptides, and urea indicates moderate bioavailability of these fractions to microbes and plants. We conclude that strong sorption of protein to the solid phase limits its bioavailability and represents a rate limiting step in DON turnover.

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.

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