Contrasting effects of siderophores pyoverdine and desferrioxamine B on the mobility of iron, aluminum, and copper in Cu-contaminated soils

Highlights

• DFOB supply did not increase the mobility of Cu in soil whereas Pvd did.

• DFOB and Pvd mobilized metals in soil mainly through a ligand-controlled mechanism.

• The soil Cu contamination level altered the metal mobilization efficiency of DFOB and Pvd.

• DFOB and Pvd efficiency in mobilizing Fe and Al decreased over time.

• Pvd degradation partly contributed to reducing Pvd mobilization efficiency over time.

Abstract

Siderophores are biogenic metallophores that can play significant roles in the dynamics of a range of metals, including Cu, in the soil. Understanding the impact of siderophores on the mobility and the availability of metals in soil is required to optimize the efficiency of soil remediation processes such as phytoextraction. This study compared the ability of siderophores desferrioxamine B (DFOB) and pyoverdine (Pvd) to mobilize metals in a series of Cu-contaminated soils, and investigated the extent their metal mobilization efficiency changed over time and with the level of Cu contamination of the soil. Siderophores were supplied (or not) to Cu-contaminated soils and metal mobility was assessed through their total concentration in 0.005 M CaCl₂ extract. DFOB selectively mobilized Fe and Al while Pvd also mobilized Cu and Ni, Co, V and As but to a lesser degree. The 1:1 relationship between DFOB in the CaCl₂ extract and Fe + Al mobilized from the solid phase suggests that DFOB mobilized metals by ligand-controlled dissolution. The accumulation of Cu in soil enhanced the adsorption of DFOB and Pvd at the surface of soil constituents and the mobilization of Fe to the detriment of Al by the two siderophores. The metal mobilization efficiency of DFOB and to a lesser extent of Pvd decreased over 22 days. According to ¹⁵N-Pvd analyses, Pvd degradation at least partly contributed to the progressive reduction in the metal mobilization efficiency of Pvd. The processes behind these results and the relevance of these results for manipulating the availability of Cu (and Fe) in soil are discussed.

Introduction

Copper is a major component of crop protection methods against fungi and bacteria as it is the only active substance allowed in organic farming that has both a strong biocidal effect and a wide range of action (Andrivon et al., 2017). Copper is used to prevent a variety of crop diseases including mildew, some fungal diseases and most bacterial diseases, particularly on grapevines, and on fruit and vegetable crops (Andrivon et al., 2017). The two main crop diseases, in terms of planted area and economic importance, for which Cu is used are downy mildew of vine caused by the oomycete Plasmopara viticola and apple scab caused by the ascomycete Venturia inaequalis (Andrivon et al., 2017). The soil of many vineyards and orchards is contaminated by Cu due to the long-term use of Cu-based fungicides such as Bordeaux mixture. Copper contamination is particularly high in old vineyards (Komarek et al., 2010, Mackie et al., 2012) and in old orchards (Zhou et al., 2011, Wang et al., 2015) where the concentration of Cu in the topsoil (0–20 cm) can reach several hundred mg kg⁻¹ soil.

Soil Cu contamination in vineyard and orchard soils, although moderate compared to that of Cu-polluted soils located near Cu mines (Zotti et al., 2014), Cu smelting factories (Wang et al., 2014) or at wood preservation sites (Kolbas et al., 2020), has consequences for the functioning and the sustainability of these ecosystems since it has chronic effects on the dynamics of soil populations. Karimi et al. (2021) performed a meta-analysis of Cu ecotoxicity and reported that Cu harms soil microorganisms at concentrations above 200 kg Cu ha⁻¹ (Cu of 67 mg kg⁻¹ soil), which is currently the level found in many vineyard and orchard topsoils. Excess Cu reduces microbial activity (Soler-Rovira et al., 2013) and biodiversity (Viti et al., 2008) in vineyard topsoils, and reduces microbial biomass and C mineralization rates in apple orchard topsoils (Wang et al., 2009). Ways to reduce the Cu contamination of vineyard and orchard soils are thus needed along with the use of other substances than Cu to protect vines and fruit trees against bacterial and fungal diseases.

Phytoextraction progressively reduces the concentration of metals in soil by accumulating metals in harvestable plant parts (Bert, 2013). Copper phytoextraction is still in the experimental stage as yields do not yet reduce soil Cu contamination sufficiently. The limited phytoavailability of Cu in vineyard or orchard soils (e.g. compared to Ni in serpentine soils) and its preferential accumulation in the roots of most Cu-extracting plants makes phytoextraction of even 1 kg Cu ha⁻¹ year⁻¹ difficult. One way to increase Cu phytoavailability in the soil without causing Cu leaching to groundwater is to inoculate the rhizosphere of the Cu-accumulating plant with siderophore producing bacteria (SPB). Siderophores are biogenic metallophores released by some plants (e.g. Poaceous species), soil fungi (e.g. Aspergillus) and soil bacteria (e.g. Streptomyces, Pseudomonads) to guarantee their iron nutrition under iron starvation. Although siderophores are generally considered as biological iron uptake agents, they can form stable complexes (Braud et al., 2010) and play a significant role in the biogeochemical cycling of a range of metals, including Cu (Kraemer et al., 2015). Previous studies (Cornu et al., 2014; 2019) revealed for instance, that the mixed catecholate and hydroxamate siderophore pyoverdine (Pvd) enhanced the mobility (i.e. the solid-solution transfer) of Cu in vineyard soils. However, the in situ deployment of bioaugmentation-assisted phytoextraction for Cu requires a better understanding of the processes used by siderophores to mobilize Cu in soil, in order to identify the conditions (type of siderophore, soil characteristics, etc.) needed to optimize their efficiency.

Batch experiments showed that mineral Fe-bearing phases (Fe oxyhydroxides, clays) dissolve almost exclusively via a ligand-controlled dissolution mechanism in presence of siderophores (Cheah et al., 2003, Kraemer, 2004, Akafia et al., 2014). This means that the siderophore-promoted mobilization of Fe primarily relies on Fe complexation by siderophores, in solution and at the mineral surface, which increases both the solubility and the dissolution rate of mineral Fe-bearing phases. However, this theoretical model does not necessarily apply to Cu, because Cu and Fe do not have the same geochemistry, or to soils, because minerals in soils are associated with solid organic matter, and metals and metallophores (other than siderophores) are present in large numbers.

The aim of the present study was to better understand the processes used by siderophores to mobilize metals in soils. The first objective was to investigate the relationship between the complexation and the mobilization of metals in soil by comparing the efficiency of Cu mobilization of two siderophores with contrasting stability constants for Cu(II): desferrioxamine B (DFOB) and Pvd. The second objective was to test whether the level of soil contamination by Cu affects the efficiency of DFOB and Pvd in mobilizing metals in soil. The third objective was to assess the duration of the siderophore effect on the mobility of metals in the soil by monitoring changes in the metal mobilization efficiency of DFOB and Pvd over time.