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

Oriane Della-Negra (1) , Sébastien Chaussonnerie (1) , Nuria Fonknechten (1) , Agnès Barbance (1) , Delphine Muselet (1) , Déborah Martin , Stéphanie Fouteau (1) , Cécile Fischer , Pierre-Loïc Saaidi (1) , Denis Le Paslier (1)

1 UMR 8030 - Génomique métabolique

The insecticide chlordecone has been used in the French West Indies for decades, resulting in long term pollution, human health problems and social crisis. In addition to bacterial consortia and Citrobacter sp.86 previously described to transform chlordecone into three families of transformation products (A: hydrochlordecones, B: polychloroindenes and C: polychloroindenecarboxylic acids), another bacterium Desulfovibrio sp.86, showing the same abilities has been isolated and its genome was sequenced. Ring-opening dechlorination, leading to A, B and C families, was observed as previously described. changing operating conditions in the presence of chlordecone gave rise to the formation of an unknown sulfur-containing transformation product instead of the aforementioned ones. Its structural elucidation enabled to conclude to a thiol derivative, which corresponds to an undocumented bacterial reductive sulfidation. Microbial experiments pointed out that the chlordecone thiol derivative was observed in anaerobiosis, and required the presence of an electron acceptor containing sulfur or hydrogen sulfide, in a confined atmosphere. It seems that this new reaction is also active on hydrochlordecones, as the 10-monohydrochlordecone A1 was transformed the same way. Moreover, the chlordecone thiol derivative called F1 was detected in several chlordecone contaminated mangrove bed sediments from Martinique Island, highlighting the environmental relevance of these results. Chlordecone is a highly recalcitrant organochlorine pesticide that has been added to the Stockholm convention list of persistent organic pollutants in 2009. Several pest control products containing chlordecone (Kepone, Curlone) or a functionalized derivative (Kelevan) have been manufactured in the US, Brazil and France and applied in the Caribbean, Central America, West Africa, and Europe over an extended period of forty years 1. To date, chlordecone has caused two major environmental disasters: (1) acute exposure of workers at the Hopewell (US) chlordecone production plant in 1975 and massive pollution of the James River, extending over 100 miles that lasted for decades 2 , (2) ongoing impregnation of the French West Indies (FWI) population due to extensive agricultural use of chlordecone from 1972 to 1993 that has resulted in long-term pollution of environmental compartments (soils, water resources, coastal areas) and subsequently of some local food production (vegetables, farmed animals, and seafood). Until now, no remediation strategy has been proven satisfactory in the FWI environment whereas the population has to deal with health troubles (increased risk of cancer, motor and cognitive development disorders in young children, premature births) and social difficulties (disappearance of local economy activities) 1 .

Domaines: Bactériologie; Chimie analytique

Oriane Della-Negra, Sébastien Chaussonnerie, Nuria Fonknechten, Agnès Barbance, Delphine Muselet, et al.. Transformation of the recalcitrant pesticide chlordecone by Desulfovibrio sp.86 with a switch from ring-opening dechlorination to reductive sulfidation activity. Scientific Reports, 2020, 10 (1), ⟨10.1038/s41598-020-70124-9⟩. ⟨hal-02998150⟩