Fate of lignins in soils: A review

Soil Biology & Biochemistry 42 (2010) 1200e1211

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Review

Fate of lignins in soils: A review Mathieu Thevenot*, Marie-France Dignac, Cornelia Rumpel UMR Biogéochimie et Ecologie des Milieux Continentaux (BioEMCo), INRA-CNRS-INAPG-ENS-ENSCP-Univ. Paris VI, Bâtiment EGER, 78850 Thiverval-Grignon, France

a r t i c l e i n f o

a b s t r a c t

Article history: Received 7 April 2009 Received in revised form 22 March 2010 Accepted 24 March 2010 Available online 9 April 2010

Lignins are amongst the most studied macromolecules in natural environments. During the last decades, lignins were considered as important components for the carbon cycle in soils, and particularly for the carbon storage. Thus, they are an important variable in many soileplant models such as CENTURY and RothC, and appeared determinant for the estimation of the soil organic matter (SOM) pool-size and its stabilization. Recent studies challenged this point of view. The aim of this paper was to synthesise the current knowledge and recent progress about quantity, composition and turnover of lignins in soils and to identify variables determining lignin residence time. In soils, lignins evolve under the influence of various variables and processes such as their degradation or mineralization, as well as their incorporation into SOM. Lignin-derived products obtained after CuO oxidation can be used as environmental biomarkers, and also vary with the degree of degradation of the molecule. The lignin degradation is related to the nature of vegetation and land-use, but also to the climate and soil characteristics. Lignin content of SOM decreases with decreasing size of the granulometric fractions, whereas its level of degradation increases concomitantly. Many studies and our results suggest the accumulation and potential stabilization of a part of lignins in soils, by interaction with the clay minerals, although the mechanisms remain unclear. Lignin turnover in soils could be faster than that of the total SOM. Different kinetic pools of lignins were suggested, which sizes seem to be variable for different soil types. The mechanisms behind different degradation kinetics as well as their potential stabilization behaviour still need to be elucidated. Ó 2010 Elsevier Ltd. All rights reserved.

Keywords: Review Lignin turnover Carbon dynamics Soil organic matter

1. Introduction Lignins are the most abundant aromatic plant component in terrestrial ecosystems and represent a significant part of plant litter input (approximately 20%) into soils (Crawford, 1981; KögelKnabner, 2000; Gleixner et al., 2001). In higher plants, lignins are chemically connected to cellulose and hemicellulose in the cellulosic fiber walls, providing strength and rigidity to the plant structures as well as resistance to the biodegradation of carbohydrates (i.e., enzymatic hydrolysis) and to environmental stresses (Brown, 1961; Kirk and Farrell, 1987; Argylopoulos and Menachem, 1997; Higuchi, 1998, 2006). Lignins are synthesized from L-phenylalanine and cinnamic acids via various metabolic ways to form lignin precursors such as sinapyl and coniferyl alcohols (Schubert and Acerbo, 1959; Higuchi and Barnoud, 1964; Higuchi, 1971). The lignin structure consists of aromatic rings with side chains and eOH and eOCH3 groups linked * Corresponding author. Present address: Laboratoire de Génie Civil et GéoEnvironnement (LGCgE), Université Lille1, Bâtiment SN5, 59655 Villeneuve-d’Ascq Cedex, France. E-mail address: [email protected] (M. Thevenot). 0038-0717/$ e see front matter Ó 2010 Elsevier Ltd. All rights reserved. doi:10.1016/j.soilbio.2010.03.017

by various strong covalent bonds (alkyl-aryl ether and CeC). Lignins are synthesized by oxidative copolymerization of three p-hydroxycinnamyl alcohols (p-coumaryl, coniferyl and sinapyl), which contribute in varying proportions to the macromolecular structure depending upon the morphological parts of plants (Freudenberg, 1956; Adler, 1977). Due to the high soil input and the abundance of aromatic structures suggesting chemical recalcitrance, until recently, lignins were considered as a major component of soil organic matter (SOM), influencing its pool-size and its turnover. Lignins are used as input criterion in many soileplant models, such as CENTURY, RothC and Daisy, to estimate SOM dynamics. In these models, lignin concentration is used as an initial compartment and/or as a variable to distinguish SOM compartments with different dynamics (metabolic, structural and recalcitrant/passive). Moreover, various fluxes between SOM compartments are modeled notably using the ‘lignin’ variable. However, recent evidences suggest that the stability and low degradability of lignins in soils seems to be overestimated and their contribution to humus exaggerated (Stevenson, 1994). To give an overview of the findings and research needs concerning lignin composition and turnover in soils, we carried out an exhaustive study of the international literature. Three principal and

M. Thevenot et al. / Soil Biology & Biochemistry 42 (2010) 1200e1211

determining points were addressed: 1. the source and degradation of lignins (i.e., alteration of chemical structure and mineralization) in different soil types, and under different climates and land-uses, 2. their distribution with soil depth and in particle-size fractions as influenced by soil properties and climate, and 3. the dynamics of specific lignin-derived compounds in soils. In our review, the fate of lignins has been addressed with regards to studies using cupric oxide (CuO) oxidation and gas-chromatographic analysis of the phenolic CuO-oxidation products. Indeed, this method is commonly used for the characterization and quantification of lignins in soils. CuO oxidation yields a suite of single-ring phenol compounds (V: vanillyl, S: syringyl and C: cinnamyl) with their aldehyde, ketone and acid substitutions (Fig. 1). These compounds are generally used as biochemical indicators of origin and state of decomposition of lignin and SOM. The sum (V þ S þ C) and various characteristic ratios, such as the Acid-to-Aldehyde ratios (Ad-to-Al) and the C- or S-to-V ratios, can be calculated. The VSC sum is generally considered as quantitative measure of soil lignin, whereas (Ad-to-Al) ratios are indicators of the state of lignin degradation in soil. With increasing decomposition, VSC is usually decreasing, whereas the (Ad-to-Al) ratios of V and S units are increasing. C- and S-to-V ratios are often used as source indicators. 2. Lignins in soils: sources and transformations 2.1. Lignins as source markers Wood and vascular tissues generally contain 20e30 g kg1 of lignin (Kirk and Farrell, 1987). Whittaker and Likens (1975) have estimated a proportion of lignin on earth equivalent to 3  1011 metric tons. Lignins are transferred from the plants to the soil, via

1201

aboveground (aboveground organs, i.e., shoots, leaves.) or belowground (root system) litter. Lignins mainly occur in the intracellular layers of the cambium of woody and non-woody higher plants with a vascular system, such as Gramineae or gymnosperm and angiosperm trees. The molecular composition of lignins in soils and sediments can be related to major plant groups such as angiosperms and gymnosperms (Hedges and Mann, 1979; Hedges and Ertel, 1982; Hedges and Weliky, 1989; Sanger et al., 1996; van Bergen et al., 1997; Nierop et al., 2001; Nierop and Verstraten, 2003). The relationship between the S-to-V and C-to-V ratios of soils and sediments was found to vary in accordance with their source plants, reflecting a partial preservation of characteristic lignin patterns from plants to soils and sediments (Goñi et al., 1993; Hu et al., 1999; Jolivet et al., 2001; Dittmar and Lara, 2001; Otto and Simpson, 2006). Indeed, gymnosperm and angiosperm lignin composition vary in their abundance in V, S, C phenolic units. Gymnosperm wood contains mainly V-units (about 80%) associated with C-units, while angiosperm wood is composed of approximately equivalent amounts of V and S units associated with C units as well (Hedges and Mann, 1979; Hedges and Ertel, 1982). Non-woody vascular plant tissues such as herbaceous plants, Gramineae and pine needles contain equal amounts of V, S and C units as part of the lignin macromolecule or link between carbohydrates and lignin in the ligno-cellulose complex (Iiyama and Wallis, 1988; Lam et al., 2001). The relative contribution of V, S and C units in soils and sediments may reflect the source vegetation. For example, the representation of the S-to-V vs C-to-V ratios compiled from numerous studies (Fig. 2) permits to distinguish organic matter of angiosperm and gymnosperm taxons in soils. However, this method cannot provide undisputable results about the origin of plants belonging to the same

Fig. 1. Lignins monomers released with the alkaline CuO oxidation: H-type, V-type, S-type and C-type phenols.

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M. Thevenot et al. / Soil Biology & Biochemistry 42 (2010) 1200e1211

6 angiosperm gymnosperm

5

S-to-V

4 3 2 1

2.2. Chemical indicators of lignin alteration

0

C-to-V Fig. 2. S-to-V vs C-to-V ratios measured for angiosperm and gymnosperm plants, without distinction between organs (wood, root, leaves and stem). The data were compiled from eight studies (Hedges and Mann, 1979; Hedges et al., 1985; Alberts et al., 1991; Jolivet et al., 2001; Lobe et al., 2002; Bahri et al., 2006; Otto and Simpson, 2006; Heim and Schmidt, 2007b).

taxon (Fig. 3). This limitation may be related to the overlapping between plant molecular signature and to soil-dependant structural changes of that signature during degradation (Dümig et al., 2009). Furthermore, the lignin composition of plant input was mostly studied in forest litter layer (i.e., aboveground material), whereas various authors suggest that roots might be major contributors to lignin input to soils (Nierop et al., 2001; Abiven et al., 2005; Otto and Simpson, 2006; Feng and Simpson, 2007). In addition, the similarity between lignin compounds and the aromatic constituents of suberins, mainly present in the underground input, could further limit the taxonomic use of the CuO products.

4.0 3.5 3.0

grass maize wheat sunflower

2.5 S-to-V

In addition to lignin structural units, the composition of dimeric lignin phenols was found to be characteristic for the source of lignins (Goñi and Hedges, 1992; Opsahl and Benner, 1995; Dignac and Rumpel, 2006). Five different dimer types have been identified after CuO oxidation (5,50 -ringering bonds, 1-diketone, 1monoketone, 5-monoketone and 2-methyl side chainering bonds) (Goñi and Hedges, 1992). We can also quote the dibenzodioxocin and spirodienone structures identified by NMR from lignins as other types of linkages (Karhunen et al., 1995; Zhang et al., 2006; Rencoret et al., 2009). The dimer-to-monomer (D-to-M) ratio and some dimer ratios (side chainering dimers/ringering dimers) have been found to vary according to the plant sources (Goñi and Hedges, 1992; Otto and Simpson, 2006).

2.0 1.5 1.0 0.5 0.0 0.0 0.5 1.0 1

2.0 2.5 3.0 3.5 4.0 C-to-V

Fig. 3. S-to-V vs C-to-V ratios for various angiosperm plants, without distinction between organs (wood, root, leaves and stem). The data were compiled from eight studies (Hedges and Mann, 1979; Hedges et al., 1985; Alberts et al., 1991; Jolivet et al., 2001; Lobe et al., 2002; Bahri et al., 2006; Otto and Simpson, 2006; Heim and Schmidt, 2007b).

Due to their complex structure, only few organisms are able to degrade lignins. Lignin degradation is mainly biotic, aerobic and cometabolic (Kirk et al., 1976; Haider, 1992). Some studies suggest anaerobic biodegradation (Hackett et al., 1977; Zeikus et al., 1982; Benner et al., 1984) as well as some abiotic processes (Janshekar et al., 1981; Opsahl and Benner, 1998; Gleixner et al., 2001; Otto et al., 2005). The organisms able to degrade lignins include few bacteria such as Streptomyces sp. or Nocardia sp. (Sörensen, 1962; Trojanowski et al., 1977; Antai and Crawford, 1981; Crawford et al., 1983; Godden et al., 1992) and fungi, especially basidiomycetes brown-rot and white-rot fungi. Most of these organisms are able to alter the lignin structure, only white-rot basidiomycetes can mineralize the molecule (Trojanowski, 1969; Kirk and Adler, 1970; Crawford and Crawford, 1976; Haider and Trojanowski, 1980; Kirk and Cowling, 1984; Orth et al., 1993; Filley et al., 2002). Lignin biodegradation occurs under the action of unspecific and extracellular enzymes, such as lignin peroxidase, manganese peroxidase and laccase (Flaig, 1964; Haider and Martin, 1981; Glenn et al., 1983; Tien and Kirk, 1983; Jeffries, 1994; Hammel, 1997; Hofrichter, 2002; Higuchi, 2004). Several studies suggest the limitation or total inhibition of the lignin degradation or specific degradation pathways due to direct or indirect action of various chemical products, such as some polyphenols, o-phthalates and resins, on the total microbial and enzymatic activity (Fenn and Kirk, 1979; Forney et al., 1982; Michels and Gottschalk, 1994; Marzullo et al., 1995; Reed, 1995). Lignin biodegradation results in a decrease of the lignin concentration through mineralization, as well as through transformations (i.e., alteration of their initial structure) into non-lignin products and incorporation into SOM. The following paragraph will investigate lignin biodegradation in soils using chemical indicators after CuO oxidation. Various characteristic indicators for lignin degradation state were developed on the basis of the relative distribution of lignin phenols measured chromatographically after CuO oxidation (Table 1). Usually, VSC content decreases with increasing soil lignin degradation. However specific ratios are often preferred to V þ S þ C content since the yield of CuO oxidation might change with the degree of lignin structure alteration (Bahri et al., 2008) and for different plant species (Kögel, 1987). Due to the cleavage of the CaeCb bond of the phenylpropanoid units and oxidation of the degraded compounds, carboxylic acid units increase compared to the aldehyde ones, which leads to increasing Acid-to-Aldehyde ratios of V and S-type units upon biodegradation in soils and sediments (Ertel and Hedges, 1984; Hedges et al., 1988; Opsahl and Benner, 1995; Goñi et al., 2000; Amelung et al., 1999; Rumpel et al., 2004; Otto and Simpson, 2006). Syringyl and cinnamyl units are preferentially degraded compared to the guaiacyl units (V units), resulting in a decrease of the S-to-V and C-to-V ratio values during lignin degradation (Kögel, 1986; Goñi et al., 1993; Opsahl and

M. Thevenot et al. / Soil Biology & Biochemistry 42 (2010) 1200e1211 Table 1 Main CuO parameters used to describe the lignin degradation in soils (Ertel and Hedges, 1984; Hedges et al., 1988; Goñi and Hedges, 1992; Otto and Simpson, 2006). Parameter

Definition

VSC (in mg VSC g1 OC or Soil)

Sum of the 8 major lignin phenols (S þ V þ C)a

C-to-V and S-to-V Cinnamyl phenols- and syringyl phenols-to-vanillyl phenols Acid-to-Aldehyde ratio

a

Vanillic acid-to-vanillin Syringic acid-to-syringaldehyde p-Hydroxybenzoic acid-to-p-hydroxybenzaldehyde Dihydrodivanillic acid-to-dihydrodivanillin Dehydrodivanillin, dehydrovanillinacetovanillone, dehydrovanillinvanillic acid, dehydroacetovanillonevanillic acid, dehydrodivanillic acid-to-a,1-monoketone dimers (vanillovanillone, vanillosyringone, syringosyringone) or b,1-diketone dimers (vanillyl, vanillosyringyl, syringyl)

V: vanillyl phenols, S: syringyl phenols, C, cinnamyl phenols.

Benner, 1995; Otto and Simpson, 2006), except at the first stage of degradation (Christman and Oglesby, 1971; Kögel, 1986). The C- and S-to-V ratios are not often used as lignin degradation indicators, due to overlapping with source variation and opposite trends in the course of lignin degradation. In our review of the literature, the (Ad-to-Al) ratios of soils were in the range 0.16e4.36 for (Ad-to-Al)V and 0.22e4.67 for (Ad-to-Al)S (Fig. 4a), while they are 0.1e0.2 for fresh angiosperm wood and 0.2e1.6 for non-woody tissues (Hedges and Mann, 1979; Hedges et al., 1988; Benner et al., 1990; da Cunha et al., 2001). Higher variability was observed for soils under forest (about 0.3e4.5) compared to grassland and arable soils (about 0.2e1.0) (Fig. 4bed). The variability observed under forest could be

5

5

Grassland and pasture soils

(A d -to -A l)V

Undifferencied land use

4

4

3

3

2

2

1

1

0

0

1

2

3

4

5

0

0

1

2

3

4

5

2

3

4

5

5

5

Forest soils

Arable soils

4

4

3

3

2

2

1

1 0

0 0

1

2

3

4

5

0

1

(Ad-to-Al)S Fig. 4. Acid-to-Aldehyde ratios of vanillyl and syringyl units [(Ad-to-Al)V,S], for all the compiled studies (a) and for grassland and pasture soils (b), arable soils (c) and forest soils (d). The data were compiled from sixteen studies (Ugolini et al., 1981; Amelung et al., 1999; Jolivet et al., 2001; Six et al., 2001; Lobe et al., 2002; Rumpel et al., 2002; Solomon et al., 2002; Kiem and Kögel-Knabner, 2003; Dignac et al., 2005; Otto et al., 2005; Peinemann et al., 2005; Bahri et al., 2006; Otto and Simpson, 2006; Heim and Schmidt, 2007b; Bierke et al., 2008; Wiesmeier et al., 2009).

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explained by a higher heterogeneity of soil properties and climate (mineral composition, pH, temperature and water content) and thus conditions for lignin degradation, compared to arable and grassland soils with more homogenous conditions. The higher Adto-Al ratios recorded for forest soils might indicate a higher degree of lignin transformations, which could be explained by more favorable environmental conditions for microbial and fungal activity due to constant temperature and moisture conditions, and to lower pH values (Paul and Clark, 1989; Donnely et al., 1990; Otto and Simpson, 2006), which could have resulted in a more adapted and abundant lignin degrading microbial communities. Indeed, white-rot fungi, the main lignin degraders, have been identified in forest soils. Up to now, the lignin degraders and degradation pathways in arable soils are poorly known. Additional information on structural alteration and diagenetic state of lignin may be obtained from lignin dimers (Goñi and Hedges, 1992; Monreal et al., 1995; Opsahl and Benner, 1995; Dignac and Rumpel, 2006; Rencoret et al., 2009). For example, the (Ad-to-Al) ratio of vanillic dimers, the ratio of 5,50 -to-a,1 and of 5,50 -to-b,1, increase from plants to soils (Otto and Simpson, 2006). Dimer content in soil and litter globally increases with the organic matter decomposition, but as function of the source of the organic residues (Kögel et al., 1988; Leinweber and Schulten, 1995; Kalbitz et al., 2003). More studies are needed to explore the potential of dimers to elucidate lignin degradation pathways in soil. 2.3. Environmental parameters influencing lignin degradation In soils, it is well known that the bulk organic matter degradation is influenced by various environmental variables such as pH, soil moisture or climate. To determine the relation between chemical parameters of soils, climate and lignin degradation, we performed a principal component analysis (PCA) on the data from 12 studies for which S-to-V ratio (S-to-V), Ad-to-Al ratio of the V units ((Ad-to-Al)V), organic carbon content (OC), nitrogen content (N), OC-to-N ratio, soil pH, mean annual temperature (MAT) and mean annual precipitation (MAP) were known or could be calculated. The analysis was performed using the statistical software SPAD (SPAD 7.0, Coheris SPAD, France). The result of the PCA is given in Fig. 5. The PCA exhibits a relation between the S-to-V ratio and soil pH whereas the (Ad-to-Al)V ratio is related to the OC-to-N ratio and MAT. Thus, our result suggests that lignin alteration is influenced by soil acidity and climate, which are known to modify the biological activity (Brook et al., 1983; Amundson et al., 1989; Raich and Schlesinger, 1992; Anderson and Domsch, 1993; Andersson and Nilsson, 2001). In accordance with the results of Amelung et al. (1999), increasing temperatures would lead to a decrease of the (Ad-to-Al)V ratio, whatever the MAP. Meentemeyer (1978), Johansson et al. (1995) and Berg et al. (1993) observed a correlation between the annual actual evapotranspiration (AET) and lignin losses in litter, indicating low mass loss at high AET. The pH effect suggested by the PCA could reflect the impact of pH on the activity of fungi in soils, the optimal activity being registered around pH 5 (Kirk et al., 1978; Bending and Read, 1997). Pometto and Crawford (1986) also observed optimal pH conditions for lignin degradation by Streptomyces (pH 9.5). The lignin degradation indicator, (Ad-to-Al)V ratio, appears to be related to the OC-to-N ratio, currently assumed as a good predicator of organic matter degradation and mass loss rate (Sjöberg et al., 2004a). This could be also related to the known impact of nitrogen on lignin degradation, despite the lack of relation between the S-to-V and (Ad-to-Al)V ratios and the N content. Many authors have reported a great influence of the nitrogen on lignin degradation (Berg et al., 1982b; Berg and Ekbohm, 1991; Entry, 2000; Dignac et al., 2002). It notably appears that fungal lignin biodegradation is limited by

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M. Thevenot et al. / Soil Biology & Biochemistry 42 (2010) 1200e1211

Fig. 5. First two dimensions of the PCA performed on the data compiled from 12 studies (Amelung et al., 1999; Jolivet et al., 2001; Dignac et al., 2002; Lobe et al., 2002; Möller et al., 2002; Solomon et al., 2002; Kiem and Kögel-Knabner, 2003; Peinemann et al., 2005; Bahri et al., 2006; Otto and Simpson, 2006; Heim and Schmidt, 2007b; Wiesmeier et al., 2009). The PCA expresses the relations between the S-to-V and Acid-to-Aldehyde of vanillyl units [(Ad-to-Al)V] ratios with the OC and N contents, the OC-to-N ratio, the soil pH, the mean annual temperature (MAT) and the precipitation (MAP).

high N content (Keyser et al., 1978; Fog, 1988; Osono and Takeda, 2001) and that N concentration and sources also influence the lignin degradation by Streptomyces (Barder and Crawford, 1981). Li et al. (1994) emphasized that the N content could regulate the lignin peroxidase (LiP) gene transcription, in contrast to the result of Johnston and Aust (1994). However, other studies suggest no significant or negative impacts of N concentration on lignin degradation (Schaefer et al., 1984; Rutigliano et al., 1996; Dignac et al., 2002; Sjöberg et al., 2004b), indicating the variable influence of N and related mechanisms as function of the local conditions. In addition to these parameters, soil minerals could also influence the lignin degradation. The most important properties of the mineral phases, with respect to their influence on lignin transformations, are their effect on microbial availability of organic matter and their ability to oxidize organic compounds. Fe oxides and Al hydroxides were found to reduce lignin decomposition (Miltner and Zech, 1998). 3. Lignin distribution in soils Lignin distribution in soils is the result of input and decomposition processes, which might be influenced by soil properties and environmental conditions. 3.1. Impact of land-use and climate We performed a statistical analysis on 27 studies (Table 2) for which VSC, OC and N content, OC-to-N and VSC-to-OC ratios, clay content, soil pH, mean annual temperature (MAT) and precipitation (MAP) were known or could be estimated in order to elucidate the main environmental conditions determining lignin content in soils and SOM. Additionally we analyzed the effect of land-use (forest,

arable and grassland). The data were classified according to three categories (LOW, MEAN and HIGH) of equivalent strength, using the classification procedure of the statistical software SPAD (SPAD 7.0, Coheris SPAD, France). We obtained a new standardized matrix. The data set was analyzed by multiple correspondence analysis (MCA), which is a multivariate technique similar to PCA designed to analyze the correspondence between rows and columns of a matrix (Panagiotakos and Pitsavos, 2004). The results of the MCA are displayed in Fig. 6, presenting the first three dimensions obtained. The VSC content in soils seems to be related to the OC and N contents, as generally observed, indicating higher lignin content for forest than for arable soils. The VSC content of SOM (VSC-to-OC) is related to the clay content and climate. The higher the clay content and MAT and MAP are, the larger is the VSC content of SOM, in accordance with the result of the PCA (Fig. 5). The relationship between VSC content of SOM and land-use is less clear, but suggests a relation between land-use and lignin content and composition (Fig. 6). It is important to note that most of the studies used were performed in Europe and North America, suggesting a limited representativity of the results according to the large contrast between climate or soil properties existing worldwide. To be representative and to draw definitive conclusions about the effects of climate on the fate of lignin in soil, new data from various and contrasted sites, such as tropical zones, are necessary. The comparison of the VSC content of SOM from twenty nine studies (Fig. 7a) shows highest values in arable soils followed by grassland and forest soils. This land-use effect might be related to the difference of organic matter sources and decomposition conditions. Indeed, conditions for main lignin decomposers (white-rot fungi) are more favorable in forest soils (see Section 2.3) compared to arable soils and grassland. However, VSC content of SOM in soils under different land-use, and thus vegetation, might be related to the contrasting yields of CuO-oxidation products between vegetation types. For example VSC values for gymnosperm and angiosperm lignins are different due to the contrasting yields of CuO products depending on the relative contribution of non-oxidizable biphenyl- and phenylcoumaran bonds (Kögel, 1987). 3.2. Distribution of lignin in mineral horizons The distribution of lignins in the soil horizons has been discussed in many studies (Guggenberger and Zech, 1994; Guggenberger et al., 1994; Sanger et al., 1997a,b; Amelung et al., 1999; Rodionov et al., 1999; Möller et al., 2002; Rumpel et al., 2002; Peineman et al., 2005; Cerli et al., 2006; Otto and Simpson, 2006; Heim and Schmidt, 2007a; Wiesmeier et al., 2009), demonstrating that lignin content decreases from the litter to the A horizon and generally with depth in the subsoil. However, an increase of lignin content of SOM with depth has been observed in some cases (Sanger et al., 1997a,b; Feng and Simpson, 2007; Mason et al., 2009), which could be attributed to vertical transport and to the protection of lignins. This suggests that lignin distribution in soils could vary from one site to another and the processes involved are not yet clear. The Acid-to-Aldehyde ratios of the V and S units usually increase with soil depth, suggesting a higher state of degradation in mineral horizons than in the organic topsoil horizons, which is in accordance with the decreasing VSC-lignin contents with depth and the limited input of fresh organic material in deep soil horizons. The lignin content of SOM (VSC-to-OC) decreases from the coarse to the finest particle-size fractions (Fig. 7b). At the same time the Acid-to-Aldehyde ratios increase with decreasing particle-size and are highest in the clay fraction (Schulten and Leinweber, 1991; Guggenberger et al., 1995; Schöning et al., 2005; Spielvogel et al., 2008) (Fig. 8). The lignins present in the finest fractions seem to

M. Thevenot et al. / Soil Biology & Biochemistry 42 (2010) 1200e1211

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Table 2 Lignins and other parameters used for the multiple component analysis. All the parameters are given in mean, or ranges as reported by the respective authors. No.a

Location

Land-useb

MAT ( C)

MAP (mm)

Depth (cm)

TOC (g kg1)

Clay (g kg1)

VSC (g kg1 OC)

1

Germany

F G C

6.5

1500

A hor.

59.3e84.2 72.7 24.6

2

Colombia

S P

26.0

2200

A hor.

20.6 24.3

394 313e408

3.5 9.7e11.5

400e660

S-to-V

(Ad-to-Al)V

(Ad-to-Al)S

12.0e22.6 19.0 10.9

3

Philippines

C

0e15

13.0e28.8

0.2e1.0

1.33e2.18

2.0e3.6

0.37e0.99

4

Russia

G

5.3

573

0e10 50e60

29.0e57.1

3.4e15.0

0.55e0.90

0.23e0.35

0.36e0.49

F St

20.8e53.2 4.1e8.0

300e715

0e10 50e60

2.3e14.0 3.4e15.0

0.63e0.65 0.64e0.78

0.31e0.33 0.27e0.30

0.41e0.46 0.42e0.44

0.53e1.45

0.16e0.48

0.32e59

5

USA

G

0.9e23.4

300e1308

0e10

11.3e64.0

162e344

9.1e26.4

6

Costa Rica

F

26.0

3600

0e50

58.0e81.0

610e665

13.0e35.0

7

Kyrgyzia

F P

4.1

743

A hor.

130.8 87.7

155 199

15.0 12.0

8

Tanzania

F C

20.0

550

0e10

13.8e18.7 8.2e19.2

180e295 251

14.1e16.5 11.8e13.5

9

Nebraska

C

8.5

400

0e5

23.0

22.4

10

France

F C

0e25 0e25

34.2 19.0e23.1

7.3 7.2e7.6

0.21 0.22e0.67

1.45 1.73e3.34

11

South Africa

C

13.8e16.6

516e625

0e20

4.4e12.7

100e190

6.6e11.9

0.8e1.5

0.20e0.29

0.37e0.68

12

Norway, Germany, Denmark

F

4.5e9.0

660e2440

A hor.

17.2e165.8

15e528

6.7e16.8

0.01e0.3

0.30e0.93

0.39e3.65

13

Thailand

F F F C

25.0

1400

A hor.

61.2 50.0 40.4 43.8

401 370 533 479

5.4 10.4 16.3 10.1

0.51 0.65 0.48 0.53

0.80 0.70 0.58 0.70

14

Germany

F F

700e800 950e1250

0e150 0e80

0.5e82.6 1.9e92.8

7.8e28.0 3.1e17.2

15

Ethiopia

FeC

18.0 19.0

1800 1250

0e10

38.0e85.0 38.0e103.0

16.6e25.9 17.9e23.3

16

Germany Czech Republic Poland

C C C

6.3e8.9 8.1 7.9

490e900 450 527

0e20 0e20 0e20

3.2e48 13.0e29.0 4.4e8.8

4.6e28.9 4.6e13.2 7.8e26.0

17

Canada

G

1.7e3.3

413e452

A hor.

2.1e5.3

2.7e4.8

0.8e1.1

1.2e1.9

0.8e1.7

18

Argentina

P C

0e9 0e30 0e22

13.0e38.0 13.0e46.0

13.7e46.8 4.0e36.2

0.96e1.60 0.87e1.79

0.15e0.44 0.14e0.58

0.22e0.46 0.36e0.64

19

Italy France Denmark Germany

F F F F

Ah Ah Ah Ah

96.0 31.0 45.0 32.0e49.0

20

Canada

G GeF F

1.7e3.3

413e452

0e25

21.0e53.0 50.0e142.0 231.0

6.1e7.3

800e1050

0e30

26.0e463.0

hor. hor. hor. hor.

30e230 290 60

594 305 236 311e558

0.34 1.30

0.43

0.19e0.80 0.81e2.87

0.39e1.38

0.62e0.89 0.22e0.85

0.36e0.52 0.28e0.44

0.55e0.61 0.45e0.72

1.3e2.0 1.7e1.8 1.1e1.8

0.14e0.56 0.20e0.34 0.18e0.56

0.38e0.71 0.40e0.41 0.44e0.71

10.0 17.0 8.0 13.0e22.0

0.33 0.23 0.51 0.23e0.32

2.7e4.8 1.1e16.7 7.7

0.8e1.1 0.7e1.0 0.1e0.3

1.2e1.9 0.8e4.2 0.4e1.1

20e130

3.70e59.4

0.01e0.80

170

8.0e11.5

1.50

0.4e0.7

0.6e0.8

17.7e23.8

1.18e1.62

0.36

0.56e0.64 0.57e0.89 0.45e0.49 0.38e0.48

21

Sweden

F

22

France

C

0e25

13.5

23

Germany

C

8.7

886

0e30

11.2e11.3

24

France Germany Switzerland

C G Pots

10.5 8.8 8.6

600 698 1138

0e30 0e10 0e10

9.8e11.6 16.2e24.2 24.0e28.7

249 330e390 280

26.0e31.0 32.0e49.0 25.0e34.0

1.0 0.9e1.0 0.6e1.1

0.60e0.72 0.50e0.55 0.34e0.47

25

Germany

F

5.7

1225

Ah hor. Ah hor. Ah hor.

68.0 39.0 32.0

250 290 80

30.0 26.0 35.0

0.00 0.00 0.09

0.54 0.55 0.68

26

China

C C C

16.0 16.0 25.0

1550 1150 1900

0e20

13.0e20.0 12.0e14.0 16.0e17.0

220 190 600

24.0e33.0 42.0e48.0 50.0e64.0

0.90e1.20 1.14v1.38 1.29e1.44

0.38e0.47 0.42e0.48 0.28e0.40

Philippines

0.68

0.8e1.7 0.9e3.5 0.7e1.7

0.60e0.80 0.51e0.63 0.39e0.48

(continued on next page)

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M. Thevenot et al. / Soil Biology & Biochemistry 42 (2010) 1200e1211

Table 2 (continued ) No.a

Location

Land-useb

MAT ( C)

MAP (mm)

Depth (cm)

TOC (g kg1)

Clay (g kg1)

VSC (g kg1 OC)

S-to-V

(Ad-to-Al)V

(Ad-to-Al)S

27

Brazil

G F F

14.5

1900

0e15

112.8 78.3 61.9

511 576 480

0.9 0.7 0.5

0.74 0.60 0.47

0.62 0.79 0.76

0.79 0.94 0.92

a 1: Guggenberger et al. (1994); 2: Guggenberger et al. (1995); 3: Olk et al. (1996); 4: Rodionov et al. (1999); 5: Amelung et al. (1999); 6: Guggenberger and Zech (1999); 7: Glaser et al. (2000); 8: Solomon et al. (2000); 9: Six et al. (2001); 10: Jolivet et al. (2001); 11: Lobe et al. (2002); 12: Dignac et al. (2002); 13: Möller et al. (2002); 14: Rumpel et al. (2002); 15: Solomon et al. (2002); 16: Kiem and Kögel-Knabner (2003); 17: Otto et al. (2005); 18: Peinemann et al. (2005); 19: Schöning et al. (2005); 20: Otto and Simpson (2006); 21: Cerli et al. (2006); 22: Bahri et al. (2006); 23: Heim and Schmidt (2007a); 24: Heim and Schmidt (2007b); 25: Spielvogel et al. (2007); 26: Bierke et al. (2008); 27: Wiesmeier et al. (2009). b Each different letter represents a different land-use (C: crop; F: forest; G: grassland; P: pasture; S: savanna; St: steppe).

be more stable, slowly degraded and less altered, than those present in the coarse fraction (Amelung et al., 1999; Lobe et al., 2002). Similar relations are observed with the MCA (Fig. 6), showing that the lignin content of SOM (VSC-to-OC) is related to the clay content. This suggests the stabilization of a part of the lignins in the fine mineral fraction and particularly in the clay fraction, which could be due to physico-chemical processes, such as clayelignin binding (Anderson and Paul, 1984; Monreal et al., 1995; Grünewald

et al., 2006). However, at this time, these processes have not yet been elucidated, as for example clay minerals or Fe and Al oxides were not found to stabilize lignins in soils (Rumpel et al., 2004; Spielvogel et al., 2008). Moreover, various studies showed that the mineral-bound organic matter is generally depleted in lignin (Guggenberger et al., 1994; Kiem and Kögel-Knabner, 2003; Schöning et al., 2005; Kögel-Knabner et al., 2008). On the other hand, the absence of a relationship between lignin and soil minerals

Fig. 6. First three dimensions of the MCA performed on the data compiled from 27 studies (Guggenberger et al., 1994, 1995; Olk et al., 1996; Rodionov et al., 1999; Amelung et al., 1999; Guggenberger and Zech, 1999; Glaser et al., 2000; Solomon et al., 2000; Six et al., 2001; Jolivet et al., 2001; Lobe et al., 2002; Dignac et al., 2002; Möller et al., 2002; Rumpel et al., 2002; Solomon et al., 2002; Kiem and Kögel-Knabner, 2003; Otto et al., 2005; Peinemann et al., 2005; Schöning et al., 2005; Otto and Simpson, 2006; Cerli et al., 2006; Bahri et al., 2006; Heim and Schmidt, 2007a; Heim and Schmidt, 2007b; Spielvogel et al., 2007; Bierke et al., 2008; Wiesmeier et al., 2009). The two graphs express the relations between the VSC abundance, the VSC-to-OC ratio (VSC-to-OC), the OC and N contents, the OC-to-N ratio, the clay content, the soil pH, the mean annual temperature (MAT) and the precipitation (MAP), classified in 3 categories (LOW, MEAN and HIGH) of equivalent strength. The relation with the ‘land-use’ (Forest [F], Arable [A] and Grassland [G]) was also explored.

M. Thevenot et al. / Soil Biology & Biochemistry 42 (2010) 1200e1211

1207

2.0

a Arable soils

1.5

Forest soils

b clay

(Ad-to-Al)s

Grassland soils

1.0

0.5

coarse sand fine sand silt clay

silt fine sand

0.0 0.0

coarse sand

0.5

1.0

1.5

2.0

(Ad-to-Al)v 0

20 40 60 80 VSC content (mg VSC g-1 OC)

100

Fig. 7. Distribution of the VSC content (g VSC kg1 OC) according to the land-use (a) and in the particle-size fractions of the 0e30 cm (b). Each bar corresponds to average value calculated from the studies used and the error bars express the standard deviation. The data were compiled from twenty nine studies (Ugolini et al., 1981; Guggenberger et al., 1994, 1995; Olk et al., 1996; Amelung et al., 1999; Guggenberger and Zech, 1999; Rodionov et al., 1999; Glaser et al., 2000; Solomon et al., 2000; Jolivet et al., 2001; Six et al., 2001; Dignac et al., 2002; Lobe et al., 2002; Möller et al., 2002; Rumpel et al., 2002; Schmidt and Kögel-Knabner, 2002; Solomon et al., 2002; Kiem and Kögel-Knabner, 2003; Rumpel et al., 2004; Peinemann et al., 2005; Otto et al., 2005; Schöning et al., 2005; Bahri et al., 2006; Otto and Simpson, 2006; Heim and Schmidt, 2007a,b; Spielvogel et al., 2007; Bierke et al., 2008; Wiesmeier et al., 2009).

does not necessarily contradict the idea of lignin sorption on clay or Fe and Al oxides and hydroxides, because the ligninemineral interactions, of unknown nature and stability, might be not identified by the currently preparative and analytical methods used. Other studies suggest preferential preservation of lignins in the silt fraction (Baldock et al., 1997; Kiem and Kögel-Knabner, 2003; Heim and Schmidt, 2007a). The interaction of lignins and minerals is probably related to their degree of degradation and transformation and the mineral composition of soils (Gu and Doner, 1993; Ballif et al., 1995; Haider, 1999). Lignins, as well as lignin-like compounds, can be also present in the soil solution. Guggenberger and Zech (1994) measured a VSClignin transport in solution through the mineral horizons of a forest soil of 30 kg ha1 year1, from the surface to the deepest horizons. Lignin loss from soil was 0.2 kg ha1 year1, suggesting lignins retention or degradation and mineralization below the A horizon. Several laboratory studies showed the high sorption potential of aromatic DOM (possibly rich in lignin) (Kaiser and Zech, 1998; Kaiser and Guggenberger, 2000), despite the lake of evidence of lignin stabilization by interactions with the mineral phase. 4. Lignin degradation rate and turnover in soils Various studies were performed in order to estimate lignin degradation and turnover rates in soil compared to those of bulk

Fig. 8. Distribution of the Acid-to-Aldehyde ratios of vanillyl and syringyl units [(Adto-Al)V,S] in the particle-size of the soils, whatever the land-use. The data were compiled from eight studies (Guggenberger et al., 1995; Amelung et al., 1999; Guggenberger and Zech, 1999; Solomon et al., 2000; Lobe et al., 2002; Kiem and Kögel-Knabner, 2003; Rumpel et al., 2004; Peinemann et al., 2005).

SOC, using different experimental approaches. Laboratory incubation of synthetic 14C-DHP lignin resulted in a decrease of 19e60% of the initial amount after 13 weeks to 2 years, depending on soil properties and vegetation type (Broadbent, 1954; Mayaudon and Balistic, 1970; Haider et al., 1977; Hackett et al., 1977; Martin and Haider, 1979, 1980; Martin et al., 1980; Haider and Kladivko, 1980; Stott et al., 1983). In field studies, using the litterbag technique, degraded lignin was found to range between 48 and 87% of the initial content after 5 years for different litter types (Berg et al., 1982a; Johansson et al., 1986; Rutigliano et al., 1996; Hobbie, 2000; Osono et al., 2008; Sanaullah et al., in press). Several studies suggested that the turnover of lignins might not be slower than the turnover of bulk soil organic carbon (SOC), and could be even faster. Indeed, for arable and forest soils, various observations suggest decrease of VSC similar or higher compared to that of the bulk SOC on sites with reduced organic matter input (Lobe et al., 2002; Rumpel and Kögel-Knabner, 2002; Kiem and Kögel-Knabner, 2003). In addition, studies based on NMR characterization of SOM failed to detect an enrichment of lignin-derived aromatic structures with depth in forest floor horizons (KögelKnabner, 1992), or in the clay fraction compared to the sand fraction (Oades et al., 1987), or in the mineral soil compared to the litter layers of forest soils (Dignac et al., 2002), or in stabilized SOM present in subsoil horizons (Rumpel et al., 2002), therefore not suggesting the preferential stabilization of lignins in soils. For the quantitative assessment of lignin dynamics, compound specific 13C analysis was recently introduced (Dignac et al., 2005; Heim and Schmidt, 2007b). This method was already used to trace the origin and fate of organic carbon in soils on sites with vegetation change, using of the natural isotopic difference between C4 (d13C around 12&) and C3 (d13C around 27&) plants (Cerri et al., 1985; Balesdent et al., 1987). The advantage of this approach is that it may be applied to soil under equilibrium (i.e., arable-land with C3/C4 crop succession). Moreover, artificially labeled biomass can be used to study lignin dynamics (Heim and Schmidt, 2007a;

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M. Thevenot et al. / Soil Biology & Biochemistry 42 (2010) 1200e1211

Marx et al., 2007) and their transformations (Bahri et al., 2008; Osono et al., 2008). A rapid turnover of lignin in agricultural soil was observed in several studies. Lignin turnover was found to be more rapid than bulk SOM (Dignac et al., 2005; Heim and Schmidt, 2007b) and labile SOM compounds such as proteins and polysaccharides (Gleixner et al., 2002). Based on 13C signature evolution with time of cultivation, Rasse et al. (2006) developed a kinetic model considering two pools of lignins: an undecomposed plant residue fraction with a turnover rate (k) of 1.9 year1 and a protected fraction with a turnover of 0.05 year1. The kinetics of bulk VSC measured by Rasse et al. (2006) are faster than those obtained by Lobe et al. (2002) based on the evolution of CuO-oxidation products after the conversion of a grassland to arable-land in South Africa. The difference between the kinetics obtained in the two studies could be explained by the methods used (VSC content vs 13C-isotopic signature), and/or by the difference of environmental conditions, influencing the fate of lignins in soils as shown above. Thus, in soils, the dynamics of lignins could be faster compared to that of bulk SOC, suggesting a weaker contribution of lignins to the stable carbon pool than previously reported. In contrast to these studies, Hofmann et al. (2009) showed in an outdoor pot study relative stabilization of lignins. However, the authors could not explain the mechanisms leading to this stabilization. They also estimated that 10% of the recent C4-derived lignin input was retained, in accordance with the results of Rasse et al. (2006). Thus, results on lignin dynamics in different soils are contradictory and the processes involved in lignin decomposition vs stabilization are still unclear. On this basis, the relevance of the ‘lignin’ variable in the models of soil carbon dynamics to estimate the size of various carbon pools and the fluxes between these pools need to be reconsidered. Indeed, we can suppose that the fixed values and relationships between the model components based on the ‘lignin’ variable are not representative of the field reality. With the aim of clearing up and confirming or not the existing results on lignin dynamics and possibly refine the lignin value used in the SOC models, more studies, in a variety of climatic conditions and soil types and based on the use of isotopic tracers, should be performed. 5. Conclusions Our study showed that, over the last 30 years, an important research effort was made concerning lignins, which increased our knowledge about their degradation and stabilization pathways in soils. The lignin degradation is related to the nature of vegetation and land-use, but also to the climate and soil characteristics. However, a high variation appears from one study to another, suggesting that the observed tendencies cannot be generalized. Lignin-derived CuO-oxidation products are efficient lignin biomarkers indicative of their origin and degradation state. These products can be used as markers of the nature of the vegetation and of the land-use, and also vary with soil depth and particle-size. Lignin content of SOM may be lower and its state of degradation higher in forest soils compared to grassland and arable soils. The lowest lignin content coupled with the highest degree of decomposition is present in deep soil and fine particle-size fractions. Lignin content of SOM and state of degradation seem mostly related to temperature (MAT). However, the observed tendencies cannot be generalized, notably due to a lack of data from other than humid temperate regions. Our literature review suggests the accumulation and stabilization of a part of lignins in soils. This stabilization could occur in the clay fraction, but the mechanisms remain unclear and CuO oxidation may not be the adequate procedure to study ligninemineral interactions. The 13C-isotopic approach appears efficient to precisely quantify the lignin turnover in situ. Recent results

are however scarce and contradictory, suggesting large variability of the lignin turnover rate in soils as well as the existence of two pools of lignins presenting different dynamics. Many contradictions and gaps exist in our current knowledge about the fate of lignin in soils, suggesting the necessity to pursue the researches on lignin fate. The use of the ‘lignin’ variable in current SOC dynamic models needs to be reconsidered. Indeed, if the lignin biodegradation processes seem well known, their stabilization and turnover in soils remains unclear limiting their interest to assess carbon storage in soil. Acknowledgements This study was funded by the Institut National de Recherche Agronomique (INRA). The authors would like to thank Claire Chenu, Naoise Nunan, Muhammad Sana Ullah, Cyril Girardin and Pierre Barré for their judicious comments on an earlier version of the manuscript. We would also like to express our thanks to the anonymous reviewers and Journal Editor for their constructive suggestions and helpful advice, very useful for improving this review. References Abiven, B., Recous, S., Reyes, V., Oliver, R., 2005. Mineralisation of C and N from root, stem and leaf residues in soil and role of their biochemical quality. Biology and Fertility of Soils 42, 119e128. Adler, E., 1977. Lignin chemistry-past, present and future. Wood Science and Technology 11, 169e218. Alberts, J.J., Price, M.T., Lewis, S., 1991. Lignin oxidation product and carbohydrate composition of plant tissues from the South-eastern United States. Estuarine, Coastal and Shelf Science 33, 213e222. Amelung, W., Flach, K.-W., Zech, W., 1999. Lignin in particle-size fractions of native grassland soils as influenced by climate. Soil Science Society of America Journal 63, 1222e1228. Amundson, R.G., Chadwick, O.A., Sowers, J.M., 1989. A comparison of soil climate and biological activity along an elevation gradient in the eastern Mojave Desert. Oecologica 80, 395e400. Anderson, T.-H., Domsch, K.H., 1993. The metabolic quotient for CO2 (qCO2) as a specific activity parameter to assess the effects of environmental conditions, such as pH, on the microbial biomass of forest soils. Soil Biology & Biochemistry 25, 393e395. Anderson, D.W., Paul, E.A., 1984. Organo-mineral complexes and their study by radiocarbon dating. Soil Science Society of America Journal 48, 298e301. Andersson, S., Nilsson, S.I., 2001. Influence of pH and temperature on microbial activity, substrate availability of soil-solution bacteria and leaching of dissolved organic carbon in a mor humus. Soil Biology & Biochemistry 33, 1181e1191. Antai, S.P., Crawford, D.L., 1981. Degradation of softwood, hardwood, and grass lignocelluloses by two Streptomyces strains. Applied and Environmental Microbiology 42, 378e380. Argyropoulos, D.S., Menachem, S.B., 1997. Lignin. In: Advances in Biochemical Engineering. Biotechnology 57, 127e158. Bahri, H., Dignac, M.-F., Rumpel, C., Rasse, D.P., Chenu, C., Mariotti, A., 2006. Lignin turnover kinetics in an agricultural soil is monomer specific. Soil Biology & Biochemistry 38, 1977e1988. Bahri, H., Rasse, D.P., Rumpel, C., Dignac, M.-F., Bardoux, G., Mariotti, A., 2008. Lignin degradation during a laboratory incubation followed by 13C isotope analysis. Soil Biology & Biochemistry 40, 1916e1922. Baldock, J.A., Oades, J.M., Nelson, P.N., Skene, T.M., Golchin, A., Clarke, P., 1997. Assessing the extent of decomposition of natural organic materials using solidstate 13C NMR spectroscopy. Australian Journal of Soil Research 35, 1061e1084. Balesdent, J., Mariotti, A., Guillet, B., 1987. Natural 13C abundance as a tracer for studies of soil organic matter dynamics. Soil Biology & Biochemistry 19, 25e30. Ballif, J.L., Guérin, H., Muller, J.C., 1995. Eléments d’agronomie Champenoise e Connaissance des sols et de leur fonctionnement e Rendzines sur craie et sols associés e Esquisse géomorphologique. INRA, Versailles, France. Barder, M.J., Crawford, D.L., 1981. Effects of carbon and nitrogen supplementation on lignin and cellulose decomposition by a Streptomyces. Canadian Journal of Microbiology 27, 859e863. Bending, G.D., Read, D.J., 1997. Lignin and soluble phenolic degradation by ectomycorrhizal and ericoid mycorrhizal fungi. Mycological Research 101, 1348e1354. Benner, R., MacCubbin, A.E., Hodson, R.E., 1984. Anaerobic biodegradation of the lignin and polysaccharide components of lignocellulose and synthetic lignin by sediment microflora. Applied and Environmental Microbiology 47, 998e1004. Benner, R., Weliky, K., Hedges, J.I., 1990. Early diagenesis of mangrove leaves in a tropical estuary: molecular level analysis of neutral sugars and lignin-derived phenols. Geochimica et Cosmochimica Acta 54, 1991e2001.

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