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

Abstract

Chlordecone (C10Cl10O) is a bishomocubane molecule, that has been used as pesticide, in many countries in Europe, America, and Africa, from the 1960s to 1990s. In the French West Indies, the historic use of chlordecone to control banana weevil infestations has resulted in pollution of large land areas. Although currently banned, chlordecone persists because it adsorbs strongly to soil and its complex structure is stable, particularly under aerobic conditions. A leaching model established that CLD pollution will last in French west indies soils several decades to half a millennium depending on soil type. However, abiotic chemical transformation catalyzed by reduced vitamin B12 has been shown to break down chlordecone by opening the cage structure to produce C9 polychloroindenes, and more recently these C9 polychloroindenes were also observed as products of anaerobic microbiological transformation by Citrobacter. To assess the potential for bioremediation, the anaerobic biotransformation of chlordecone by microbes native to soils from the French West Indies was investigated. Anaerobic microcosms were constructed 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 in active incubations 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 incubations. Chlordecone concentrations decreased in active microcosms as concentrations of products increased, indicating that anaerobic dechlorination processes have occurred. An crude estimation of partitioning coefficients between soil and water showed 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 showed 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.