Abstract

The historic use of chlordecone (C10Cl10O) as a pesticide to control banana weevil infestations has resulted in pollution of large land areas in the French West Indies. Although currently banned, chlordecone persists because it adsorbs strongly to soil and its complex bis-homocubane structure is stable, particularly under aerobic conditions. Abiotic chemical transformation catalyzed by reduced vitamin B12 has been shown to break down chlordecone by opening the cage structure to produce C9 polychloroindenes. More recently these C9 polychloroindenes were also observed as products of anaerobic microbiological transformation. To investigate the anaerobic biotransformation of chlordecone by microbes native to the French West Indies, microcosms were constructed anaerobically from chlordecone impacted Guadeloupe soil and sludge to mimic natural attenuation and eletron donor-stimulated reductive dechlorination. Original microcosms and transfers were incubated over a period of 8 years, during which they were repeatedly amended with chlordecone and electron donor (ethanol and acetone). Using LC-MS, chlordecone and degradation products were detected in all the biologically active microcosms. Observed products included monohydro-, dihydro- and trihydrochlordecone derivatives (C10Cl10-nO2Hn; n = 1,2,3), as well as “open cage” C9 polychloroindene compounds (C9Cl5-nH3+n n = 0,1,2) and C10 carboxylated polychloroindene derivatives (C10Cl4-nO2H4+n, n = 0–3). Products with as many as 9 chlorine atoms removed were detected. These products were not observed in sterile (poisoned) microcosms. Chlordecone concentrations decreased in active microcosms as concentrations of products increased, indicating that anaerobic dechlorination processes have occurred. The data enabled a crude estimation of partitioning coefficients between soil and water, showing that carboxylated intermediates sorb poorly and as a consequence may be flushed away, while polychlorinated indenes sorb strongly to soil. Microbial community analysis in microcosms revealed enrichment of anaerobic fermenting and acetogenic microbes possibly involved in anaerobic chlordecone biotransformation. It thus should be possible to stimuilate anaerobic dechlorination through donor amendment to contaminated soils, particularly as some metabolites (in particular pentachloroindene) were already detected in field samples as a result of intrinsic processes. Extensive dechlorination in the microcosms, with evidence for up to 9 Cl atoms removed from the parent molecule is game-changing, giving hope to the possibility of using bioremediation to reduce the impact of CLD contamination.

Highlights

  • Chlordecone (CLD) was used to control insect pests in banana plantations in the Caribbean, in Guadeloupe and Martinique from 1971 to 1993, despite being banned in the United States since 1974 [1, 2]

  • An Liquid Chromatograph (LC)-Orbitrap Mass Spectrometry (MS) method was eventually developed for small volume samples, where we found that the choice of extractive co-solvent was critical to the detection of both polar and non-polar metabolites

  • To provide an overview of how each set of microcosms was treated over the course of about 3000 days (~8 years), cumulative CLD and electron donor amendments were plotted over time (S2 Fig in S1 Data; with data in S4 Table)

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Summary

Introduction

Chlordecone (CLD) was used to control insect pests (mainly the banana weevil) in banana plantations in the Caribbean, in Guadeloupe and Martinique from 1971 to 1993, despite being banned in the United States since 1974 [1, 2]. This pesticide was used in the USA, as well as in some countries of Africa (Cameroon, Ivory Coast), latin America (Panama, Honduras, Equator, Nicaragua) and Asia [3,4,5]. Effective methods to decontaminate soil and protect downgradient environments, food and water supply are clearly needed

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