Contrasting effects of siderophores pyoverdine and desferrioxamine B on the mobility of iron, aluminum, and copper in Cu-contaminated soils
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.
Section snippets
Material and methods
The study was based on three experiments, each one designed to address a specific objective. Experiment 1 was designed to evaluate the effect of a supply of DFOB on the mobility of metals in a series of 14 Cu-contaminated soils. Experiment 2 was designed to test whether the level of Cu accumulation in soil is likely to alter the metal mobilization efficiency of DFOB and Pvd. This experiment was based on soil L whose original concentration of Cu (100 mg Cu kg−1) was artificially increased by
DFOB selectively promoted the mobility of Fe and Al in soil
Experiment 1 revealed that adding DFOB increased the mobility of Fe and Al in a wide range of soils and over a wide range of soil pH (5.9 < pHwater < 8.6). The concentrations of total Fe (Fig. 1a) and total Al (Fig. 1b) in the CaCl2 extract were always higher in soils supplied with DFOB than in control soils. The DFOB-promoted mobilization of Fe and Al was observed in both carbonate (F-M) and non-carbonate (A-E, N) soils. This is a crucial point since siderophores are produced only when Fe
Conclusions
The three experiments conducted in this study provide new insights into the metal mobilization ability of siderophores in soil that determines the conditions in which siderophore-producing bacteria can improve the remediation of Cu-contaminated soils through phytoextraction. First, this study highlighted the fact that the panel of metals mobilized by Pvd is larger than the panel mobilized by DFOB. Only Pvd mobilized Cu, thereby supporting the idea of using Pvd-producing bacteria (or more
Declaration of Competing Interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Acknowledgements
This work was financially supported by the French National Institute for Agriculture, Food and Environment (INRAE), by the Bordeaux wine inter-professional council (French acronym CIVB) under the EXTRACUIVRE project, by the French Agency for Environment and Energy Management (French acronym ADEME) under the VITALICUIVRE project, and by the “Pays de la Loire” regional council (France) under the OSUNA-POLLUSOLS project. The authors are grateful to L. Denaix and M. Mench for collecting and
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2023, Journal of Environmental ManagementCitation Excerpt :This is one reason why NTA mobilized Cu and Zn more efficiently than DFOB in soil, even though the affinity of NTA for these metals is similar (for Zn) or even lower (for Cu) than that of DFOB (Neubauer et al., 2002). Although the affinity for Cu of the SHS present in the ACT is probably much lower than that of pyoverdine – the log K value determined by Li et al. (2021) for complexes between Cu and SHS extracted from pig compost are within the range 4.7–6.1 – the supply of ACT increased the mobility of Cu in proportions similar to those observed for Pvd in vineyard soils (Cornu et al., 2019, 2022). In our view, the ability of ACT to mobilize Cu in soil results from its high concentration of SHS, and from the limited sorption to the solid phase of the SHS it contains (suppl. Fig F5).
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