Evaluation of the ecotoxicological impact of the organochlorine chlordecone on soil microbial community structure, abundance, and function.

Abstract

The insecticide chlordecone applied for decades in banana plantations currently contaminates 20,000 ha of arable land in the French West Indies. Although the impact of various pesticides on soil microorganisms has been studied, chlordecone toxicity to the soil microbial community has never been assessed. We investigated in two different soils (sandy loam and silty loam) exposed to different concentrations of CLD (D0, control; D1 and D10, 1 and 10 times the agronomical dose) over different periods of time (3, 7, and 32 days): (i) the fate of chlordecone by measuring (14)C-chlordecone mass balance and (ii) the impact of chlordecone on microbial community structure, abundance, and function, using standardized methods (-A-RISA, taxon-specific quantitative PCR (qPCR), and (14)C-compounds mineralizing activity). Mineralization of (14)C-chlordecone was inferior below 1 % of initial (14)C-activity. Less than 2 % of (14)C-activity was retrieved from the water-soluble fraction, while most of it remained in the organic-solvent-extractable fraction (75 % of initial (14)C-activity). Only 23 % of the remaining (14)C-activity was measured in nonextractable fraction. The fate of chlordecone significantly differed between the two soils. The soluble and nonextractable fractions were significantly higher in sandy loam soil than in silty loam soil. All the measured microbiological parameters allowed discriminating statistically the two soils and showed a variation over time. The genetic structure of the bacterial community remained insensitive to chlordecone exposure in silty loam soil. In response to chlordecone exposure, the abundance of Gram-negative bacterial groups (β-, γ-Proteobacteria, Planctomycetes, and Bacteroidetes) was significantly modified only in sandy loam soil. The mineralization of (14)C-sodium acetate and (14)C-2,4-D was insensitive to chlordecone exposure in silty loam soil. However, mineralization of (14)C-sodium acetate was significantly reduced in soil microcosms of sandy loam soil exposed to chlordecone as compared to the control (D0). These data show that chlordecone exposure induced changes in microbial community taxonomic composition and function in one of the two soils, suggesting microbial toxicity of this organochlorine.