Opportunities and risks of biofertilization for leek production in urban areas: Influence on both fungal diversity and human bioaccessibility of inorganic pollutants
Graphical abstract
Introduction
Trace metal(loid) (TM) is a generic term to gather elements naturally present at a low concentration in the environment (geochemical background). Metalloids are elements presenting properties in between those of metals and non-metals, as it is the case of antimony (Sb). Numerous human activities induce significant persistent TM contamination at the global scale by impacting the natural flows. This soil and water contamination is a major environmental issue and in particular, (peri)urban soils are widely polluted with cadmium (Cd) and lead (Pb) worldwide (Hu et al., 2014) and more recently with Sb (Krachler et al., 2005, Smichowski, 2008). Indeed, in the past decades, vehicle exhaust from lead gasoline combustion was a major source of Pb contamination (Robbins et al., 2010) and nowadays smelter areas are important sources of pollution (Zhuang et al., 2009). Cadmium accumulation in cultivated soils mostly comes from phosphate fertilizer usage (Schroeder and Balassa, 1963, Shahid et al., 2016). Antimony is a metalloid which normally occurs as a trace element in soils (He et al., 2012, Wilson et al., 2010) and is classified as a priority pollutant by the European Union (Filella et al., 2002) and the United States Environmental Protection Agency (USEPA, 2006). Although its concentration is highly variable worldwide, a 50% increase has been recorded in arctic snow in the last three decades, mainly from anthropogenic sources (Krachler et al., 2005). Smelting, mining and its presence in fire retardant mixtures are currently the most important sources of Sb. However, in the last decades, its presence in plant protection products manufacture and sewage sludge (Wagner et al., 2003, Edwards et al., 1995) has led to large-scale contamination of agricultural lands. In recent times, Sb has also been used in brake linings, lubricant and battery manufacturing (Fujiwara et al., 2011, Wiseman et al., 2013), leading to an increased risk near roads due to traffic dust. The recent conclusions of the ANSES (French National agency for food, environment and work safety) highlighted the need to strengthen research on these elements as their concentration in food increased between two sets of studies (2000–2004 and 2006–2010). These studies showed that in addition to an increase in Sb, Cd increased by up to 400% in the main food chain products, while Pb decreased a little but its concentrations remained of concern.
The worldwide economic crisis has driven more people to grow their own food in public, associative or kitchen gardens (Galt et al., 2014). However, these places are generally set-up in the vicinity of roads or industries or even directly in disused and not always cured industrial sites (Álvarez-Ayuso et al., 2012). In these strongly anthropogenic urban environments, soils and plants are consequently subjected to a high contamination risk through soil and amendment quality or airborne particles enriched with metal(loid)s (Leveque et al., 2013, Shahid et al., 2013).
Because food is the major exposure pathway for humans to environmental pollutants (Fries, 1995), metal(loid) transfer in the soil-plant-water system is often studied (Okkenhaug et al., 2011, Wan et al., 2013, Khan et al., 2016). Mycorrhizal symbiosis is the normal condition for approximately 85% of flowering plants (Brundrett et al., 1991). Both organisms benefit from this mutualistic exchange: arbuscular mycorrhizal fungi (AMF) transfer nutrients, mostly phosphorus, and can enhance stress tolerance (drought, pathogens…) (Li et al., 2013, Smith and Smith, 2011), while plants give back photosynthetic-based organic compounds to the fungus (Smith and Smith, 2011, Cazzato et al., 2012). The AMF are also known to be key actors in TM phytoavailability (Jarrah et al., 2014, Khan, 2005), while gardeners can already use them as bio-fertilizers (Kangwankraiphaisan et al., 2013). Pb behavior in the presence of mycorrhizal plants has been described (Jarrah et al., 2014), but has not yet been studied in leek, a widely cultivated vegetable (FranceAgriMer, 2013). Under metal(loid) stress, other leafy vegetables such as lettuce have been shown to accumulate high Pb levels, particularly in leaves (Beavington, 1975, Uzu et al., 2010, Xiong et al., 2014a). The relationship between Cd and AMF has been extensively studied for years, with either a decrease or an increase in accumulation depending on the fungal species, plant species and Cd concentration (Pierart, 2016). However, there are no reports about the human bioaccessible fraction of these TM in edible plants. As shown by Pierart et al., (2015), data about the relationship between Sb and AMF are very scattered. Different studies revealed Cd, Pb and Sb (eco)toxicity (Bech et al., 2012, Gebel et al., 1998, Kuroda et al., 1991, Pant et al., 2014, Winship, 1987). Both Pb and Sb have generally low solubility and bioavailability, while Cd is generally considered as highly mobile and bioavailable (Shahid et al., 2016). However, soil physico-chemical properties (i.e. organic matter, pH, Fe/Al oxides and hydroxides amounts) can affect these parameters (Xu et al., 2011, Diemar et al., 2009, Roper et al., 2012, Tighe et al., 2005, Xi et al., 2010, Ilgen and Trainor, 2012) as AMF can also influence them.
In that context, our study aims to evaluate the role of AMF fertilization in the phytoaccumulation of Cd, Pb and Sb depending on their origin (anthropic vs geogenic). Leek (Allium porrum L., Poireau de Saint Victor, Ferme de Sainte Marthe®) was chosen as a leafy vegetable model plant because it is commonly grown in urban gardens for fresh and cooked consumption (Guitart et al., 2014). The TM content analyses were performed in plant organs with the adapted extraction procedure (Okkenhaug et al., 2011). Furthermore, because the fungal community could influence metal(loid) fate at the soil-plant interface (Tonin et al., 2001), we used high throughput sequencing (illumina Miseq®) focused on a commonly studied ribosomal region, the Internal transcribed spacer (ITS) (Jansa et al., 2002, Schoch et al., 2012), to analyze its composition in leek roots.
Section snippets
Study site
Two polluted soils with similar Pb concentrations, but different contamination origins were used in the study (Table 1): (i) an urban garden sandy soil from West France (Nantes, annotated NTE: 47°16′1.512″N–1°34′29.688″O) with a high geochemical Pb anomaly, a moderate Sb anomaly and a very low Cd concentration and (ii) a peri-urban sandy-clay soil (Bazoches, annotated BZC: 48°11′21.375″N–2°3′28.993″O) in which Pb, Cd and Sb were shown to come from recent anthropic contamination (50 years) (
Results
Leek plants were cultivated on TM contaminated soils. Half of the plants received no fertilization (control; CTR) while in the other half, local AMF were added as biofertilizer to assess their effect on the soil-plant transfer of TM and their human bioaccessibility in edible organs. Plants were harvested after 25 weeks of cultivation to compare Cd, Sb and Pb accumulation in edible parts. Leek roots were used to study the fungal community and metal compartmentation on considered samples.
Antimony
Previous studies focused on Sb accumulation in leafy vegetables such as leek from contaminated soils are scattered (Kouimtzis et al., 1992). It has been shown that its accumulation in edible plants is highly variable and some vegetables such as spinach can be hyperaccumulators (Pierart et al., 2015). Kouimtzis et al., (1992) showed that compared to lettuce, leek appeared not to be a hyperaccumulator (~ 0.2 mg·kgDW− 1), which is consistent with our results, although our range of concentrations was
Conclusions and perspectives
Our results indicate that TM species and origin (anthropic or geogenic) strongly influenced TM phytoaccumulation as we observed differences in results obtained for each TM and soil.
Biofertilization efficiency appeared to be both TM and soil dependent, making results hard to interpret and to generalize as the overall context strongly influences the mechanisms involved. In addition, the developed fungal community in the BS and the changes in fungal communities in soil when applied would need to
Acknowledgments
The National Research Agency supported this work under reference ANR-12-0011-VBDU. The authors thank Elise Gay, for her precious help and support on fungal community analysis, and David Baqué for technical support on mass spectroscopy analysis. We also thank Leigh Gebbie for her thorough English revision of the present manuscript.
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LRSV, Laboratoire de recherche en sciences végétales, 24 chemin de Borderouge, 31,326 Castanet-Tolosan, France.