Immediate and long-term effect of tannins on the stabilization of soil aggregates

Highlights

• Tannins alone did not modify soil aggregate stability.

• Tannins enhanced the stabilizing role of the BSA model protein.

• Tannins reduced the stabilizing role of the polysaccharide PGA.

• Tannins prolonged the stabilizing effect of the BSA protein.

• Tannin chemical properties impacted soil physical properties.

Abstract

Soil aggregates are organomineral associations with a fundamental importance for soil structure and function. Litter from vegetation alters aggregate formation and stability, and polyphenols such as tannins found in leaves, roots and wood play an important role in soil biogeochemical and biological processes. However, the effect of tannins on soil physical properties remains largely unexplored. We hypothesized that tannins influence aggregate stability through their ability to (i) complex proteins in the soil and (ii) perturb the gelling property of root mucilage. Therefore, Mediterranean soil aggregates were incubated with condensed tannins, either as a pure substrate or in combination with a standard protein (bovine serum albumin, BSA) and with a model root mucilage polysaccharide (polygalacturonic acid, PGA) able to form gel-like structures with divalent cations (notably Ca²⁺) widely present in Mediterranean calcareous soils. The changes in aggregate stability were monitored under controlled conditions, immediately after the addition of tannins, after 2 weeks, 3 and 6 months of incubation. Tannins added alone did not yield a significant effect on aggregate stability. However, modulatory effects were found when combinations of treatments occurred. Tannins positively modulated the stabilizing effect of the BSA, giving credit to our hypothesis on the stabilizing role of the tannin-protein complex forming macromolecules, thus enforcing soil particle cohesion within aggregates. However, tannins negatively altered the stabilizing effect of PGA, suggesting that the expected perturbation of the PGA gelation occurred, with detrimental consequences for aggregate stability. Over time, tannins maintained the effect of BSA, suggesting a protective effect of tannins, possibly linked to their ability to slow down the degradation of nitrogen compounds through protein binding. Overall, we showed that tannins reacted with other organic compounds resulting in specific effects on physical soil properties, thus demonstrating that tannins in soils play a role beyond their effects on biogeochemical aspects.

Introduction

Aggregate stability is a key indicator of several soil properties, such as erodibility (Barthès and Roose, 2002, Ding and Zhang, 2016), carbon storage (Jastrow and Miller, 1997) or penetration by roots (Angers and Caron, 1998). Soil organic matter has been widely recognized as a major determinant of aggregate stability (Abiven et al., 2009, Le Bissonnais et al., 2007, Six et al., 2004). The influence of organic inputs depends on their nature (Abiven et al., 2009, Monnier, 1965). Certain specific organic compounds have been studied in detail, such as root and microbial polysaccharides (Chenu, 1989, Chenu et al., 1994, Schlecht-Pietsch et al., 1994, Traoré et al., 2000, Czarnes et al., 2000, Zibilske et al., 2000) or fungal-related proteins (Rillig, 2004, Wright and Upadhyaya, 1998), which are shown to have an important, positive, short to mid-term stabilizing role. In contrast, other specific compounds such as plant tannins, which are polyphenols of high molecular weight, have been poorly explored. To our knowledge, the only study on tannins showed that tannic acids prolonged the effect of polysaccharides (Griffiths and Burns, 1972). Nevertheless, tannins can be considered as good candidates for stabilizing soil aggregates for different reasons: (i) large amounts of these compounds can enter the soil from leaf and root litter (Gallet and Lebreton, 1995, Hättenschwiler and Vitousek, 2000; Kraus et al., 2003, Meier et al., 2008); (ii) tannins possess a rapid sorption ability and remain for a longer time in soils than other substances (Schmidt et al., 2012), especially condensed tannins (Nierop and Verstraten, 2006), and most importantly (iii) tannins are known to react with different classes of macromolecules, which influence aggregate stability. In particular, the reaction of tannins with proteins is known to occur through multiple hydrogen bonds and hydrophobic interactions, resulting in the formation of macromolecular cross-linked complexes (Hagermann, 1989, Hättenschwiler and Vitousek, 2000, Kraus et al., 2003). This ability of tannins to form complexes suggests a potentially important role in the stabilization of soil aggregates, through enhanced chemical bonding between organic soil compounds, and in particular proteins already present in the soil. When in contact with polysaccharides, tannins are known to perturb the gelling process of these macromolecules because of their function as proton scavengers (Wüstenberg, 2014). Therefore, tannins could also inhibit the gelling process of certain polysaccharides found in root mucilage. Polysaccharides in root mucilage react with calcium (Ca²⁺) to form gel-like structures (de Kerchove and Elimelech, 2007), with a strong positive effect on soil stability (Czarnes et al., 2000). If tannins alter mucilage properties, they will have a potentially negative effect on soil aggregate stability.

Mediterranean road embankments provide a useful terrain for exploring the links between tannins and soil aggregate stability. Sparsely covered by plants after road construction, vegetation cover of embankments then follows a successional trend with significant changes in plant community composition (Odum, 1969), resulting in the replacement of grass and herb species (generally with low tannin concentrations in leaves and roots), by small shrubs and tree species (with higher quantities of tannins). In the Mediterranean region, concentrations of tannins in plant roots were found to range from 0.2 ± 0.2 to 9.42 ± 4.4% of tannins per gram of dried roots between early (>10 years-old) and late successional plant communities (40–69 years-old) (Balmot, unpublished data). These differences in tannin concentrations should therefore result in an increase of tannins in litter and soils along a successional gradient (Nierop and Verstraten, 2006), but whether they play a role in the stabilization of soil aggregates, which also augments along successional gradients (Andres and Jorba, 2000, Erktan et al., 2016), is not known.

We explored the role of tannins in the stabilization of Mediterranean soil aggregates from road embankments and tested whether this effect varied over time. We hypothesize that tannins influence soil aggregate stability through: (i) their ability to complex proteins and (ii) their ability to perturb the stabilizing gelling property of the root mucilage analogue polygalacturonic acid (PGA). If, according to our first hypothesis, tannins enhance aggregate stability by binding proteins and other macromolecules already present in soil, then soil enrichment with proteins prior to tannin addition should result in an increased positive impact of tannins. Similarly, if, as in our second hypothesis, tannins decrease aggregate stability by perturbing the gelling of the PGA, then soil enrichment with PGA prior to tannin addition should enhance such negative modulation.

To test these hypotheses, we observed the impact of tannins on the aggregate stability of two soils from road embankments, representing early and late plant successional stages. Experiments were conducted under controlled conditions, and tannins were added either alone or in combination with protein or polysaccharide compounds.