Natural Chlordecone Degradation Revealed by Numerous Transformation Products Characterized in Key French West Indies Environmental Compartments

Abstract

Production and use of the insecticide chlordecone has caused long-term environmental pollution in the James River area and the French West Indies (FWI) that has resulted in acute human-health problems and a social crisis. High levels of chlordecone in FWI soils, even after its ban decades ago, and the absence of detection of transformation products (TPs), have suggested that chlordecone is virtually nonbiodegradable in the environment. Here, we investigated laboratory biodegradation, consisting of bacterial liquid cultures and microcosms inoculated with FWI soils, using a dual nontargeted GC-MS and LC-HRMS approach. In addition to previously reported, partly characterized hydrochlordecones and polychloroindenes (families A and B), we discovered 14 new chlordecone TPs, assigned to four families (B, C, D, and E). Organic synthesis and NMR analyses allowed us to achieve the complete structural elucidation of 19 TPs. Members of TP families A, B, C, and E were detected in soil, sediment, and water samples from Martinique and include 17 TPs not initially found in commercial chlordecone formulations. 2,4,5,6,7-Pentachloroindene was the most prominent TP, with levels similar to those of chlordecone. Overall, our results clearly show that chlordecone pollution extends beyond the parent chlordecone molecule and includes a considerable number of previously undetected TPs. Structural diversity of the identified TPs illustrates the complexity of chlordecone degradation in the environment and raises the possibility of extensive worldwide pollution of soil and aquatic ecosystems by chlordecone TPs.

Evidence for extensive anaerobic dechlorination and transformation of the pesticide chlordecone (C10Cl10O) by indigenous microbes in microcosms from Guadeloupe soil

“…In this study we relied on exact masses, unique isotope distribution patterns, and retention times to support the indentity of metabolites classes, namely hydrochlordecones, polychloroindenes, and carboxylated polychloroindenes with varying numbers of chlorine substituents. The consistency of the results with previous reports [24,33] and highly characteristic chlorine isotope pattern leave little doubt to the structure of the compounds, other than the actual position of substituents on the rings. Only purification of each compound and NMR could resolve such structural details, and these are beyond the scope of this work, and not necessary to evaluate extent of dechlorination.…”

“…The genome of the Citrobacter strain in these studies contained no reductive dehalogenase genes and thus transformation was likely cometabolic [32]. A very recent paper by the same team further identified and characterized many chlordecone transformation products [33], using chemical reduction, organic synthesis, and Nuclear magnetic resonance (NMR) spectroscopy NMR to elucidate isomer structures. Significantly, they further detected and quantified some of these same transformation products in soil samples from Martinique.…”

Transformation of the recalcitrant pesticide chlordecone by Desulfovibrio sp.86 with a switch from ring-opening dechlorination to reductive sulfidation activity

“…5, Fig. S5) were processed to recover a hierarchical clustering of environmental samples according to their taxonomic composition 6 . It was noticed that sulfate-reducing bacteria were much more present in bed sediments than in the other compartments, as previously reported [30][31][32] .…”

“…More recently, two bacterial consortia (86 and 92), isolated from microbial enrichment cultures from chlordecone-contaminated soils and wastewater treatment plant sludge, were able to transform chlordecone, under anoxic conditions, at room temperature. Several TPs were identified and grouped into three families: hydrochlordecones (family A), polychloroindenes (family B) and polychloroindenecarboxylic acids (family C) 5,6 . TPs from families B and C that were predominant arose from a ring-opening dechlorination of the chlordecone bishomocubane cage.…”

Physical limitation of pesticides (chlordecone) decontamination in volcanic soils: fractal approach and numerical simulation

“…However, a few years ago, Macarie and coworkers (Macarie et al 2016) show that there are no thermodynamic reasons for limiting the CLD degradation. Recently, Chevallier et al (2019) also found metabolites of CLD (dechlorinated CLD derivatives with loss of up to 7 Cl) in Caribbean soils. They also show that microorganisms, susceptible to degrade CLD, are present in the Caribbean soils demonstrating that natural biodegradation should be possible.…”