Abstract
Nicosulfuron is a selective herbicide belonging to the sulfonylurea family, commonly applied on maize crops. Its worldwide use results in widespread presence as a contaminant in surface streams and ground-waters. In this study, we isolated, for the first time, the Plectosphaerella cucumerina AR1 nicosulfuron-degrading fungal strain, a new record from Alnus leaf litter submerged in freshwater. The degradation of nicosulfuron by P. cucumerina AR1 was achieved by a co-metabolism process and followed a first-order model dissipation. Biodegradation kinetics analysis indicated that, in planktonic lifestyle, nicosulfuron degradation by this strain was glucose concentration dependent, with a maximum specific degradation rate of 1 g/L in glucose. When grown on natural substrata (leaf or wood) as the sole carbon sources, the Plectosphaerella cucumerina AR1 developed as a well-established biofilm in 10 days. After addition of nicosulfuron in the medium, the biofilms became thicker, with rising mycelium, after 10 days for leaves and 21 days for wood. Similar biofilm development was observed in the absence of herbicide. These fungal biofilms still conserve the nicosulfuron degradation capacity, using the same pathway as that observed with planktonic lifestyle as evidenced by LC-MS analyses. This pathway involved first the hydrolysis of the nicosulfuron sulfonylurea bridge, leading to the production of two major metabolites: 2-amino-4,6-dimethoxypyrimidine (ADMP) and 2-(aminosulfonyl)-N,N-dimethyl-3-pyridinecarboxamide (ASDM). One minor metabolite, identified as 2-(1-(4,6-dimethoxy-pyrimidin-2-yl)-ureido)-N,N-dimethyl-nicotinamide (N3), derived from the cleavage of the C-S bond of the sulfonylurea bridge and contraction by elimination of sulfur dioxide. A last metabolite (N4), detected in trace amount, was assigned to 2-(4,6-dimethoxy-pyrimidin-2-yl)-N,N-dimethyl-nicotinamide (N4), resulting from the hydrolysis of the N3 urea function. Although fungal growth was unaffected by nicosulfuron, its laccase activity was significantly impaired regardless of lifestyle. Leaf and wood surfaces being good substrata for biofilm development in rivers, P. cucumerina AR1 strain could thus have potential as an efficient candidate for the development of methods aiming to reduce contamination by nicosulfuron in aquatic environments.
Highlights
Nicosulfuron (2-[(4,6-dimethoxypyrimidin-2-yl)carbamoylsulfamoyl]-N,N-dimethylpyridine-3-carboxamide) is a sulfonylurea class herbicide used worldwide as a post-emergence herbicide to protect maize crops from weeds
The Plectosphaerella cucumerina AR1 colony showed different aspects depending on the solid culture medium used, varying from a white, fluffy and aerial mycelium in Sabouraud chloramphenicol agar medium (Figure 1E) to a beige, smooth in appearance with some white mycelia diffusing from a central dome in Potato dextrose agar (PDA) medium (Figure 1F)
Our results showed that P. cucumerina AR1 can be used to reduce nicosulfuron contamination since we demonstrated that (i) it was tolerant to nicosulfuron in contrast to what was described for other fungal species (Karpouzas et al, 2014) and (ii) it was able to degrade the nicosulfuron herbicide both in planktonic (Figure 2) and in biofilm conditions with various simple and complex carbon sources
Summary
Nicosulfuron (2-[(4,6-dimethoxypyrimidin-2-yl)carbamoylsulfamoyl]-N,N-dimethylpyridine-3-carboxamide) is a sulfonylurea class herbicide used worldwide as a post-emergence herbicide to protect maize crops from weeds. Despite the low agronomic dose recommended for nicosulfuron in crops (in Europe, 60 g active ingredient/ha; CE 1107/2009), this molecule is frequently detected in surface and ground-waters due to its high mobility, its Groundwater Ubiquity Score (GUS) being of 3.34 (Pfeiffer, 2010). This transfer can be explained by the high solubility (>7 g/L at pH ≥ 6.5) and low Kd coefficient of the molecule (ranging from 0.14 to 2.15 L/kg, Gonzalez and Ukrainczyk, 1996, 1999; Oliveira et al, 2001; Regitano and Koskinen, 2008; Trigo et al, 2014; Azcarate et al, 2015). The high detection frequency of nicosulfuron in surface waters implies chronic exposure of aquatic microbial communities and eventually a set of adaptations regarding its use by microbes
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