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

Abstract

The historic use of chlordecone (C 10 Cl 10 O) 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 bishomocubane structure is stable, particularly under aerobic conditions. Abiotic chemical transformation catalyzed by reduced vitamin B 12 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 (C 10 Cl 10-n O 2 H n ; n = 1,2,3), as well as "open cage" C9 polychloroindene compounds (C 9 Cl 5-n H 3+n n = 0,1,2) and C10 carboxylated polychloroindene derivatives (C 10 Cl 4-n O 2 H 4+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

Genetic Analysis of Citrobacter sp.86 Reveals Involvement of Corrinoids in Chlordecone and Lindane Biotransformations

“…In addition, we detected the same TPs in environmental samples from Martinique Island, suggesting that a similar natural degradation occurs in Martinique soils (Chevallier et al, 2019;Della-Negra et al, 2020). This phenomenon was independently confirmed by others with the detection of chlordecone TPs in Guadeloupe soils (Lomheim et al, 2020). However, to date, the mechanisms of chlordecone degradation remain unknown and do not seem to be mediated by organohalide-respiring bacteria.…”

“…Under biotic conditions, involvement of corrinoids as cofactors in reductive dehalogenases found in organohalide respiring bacteria that transform a variety of organochlorides pollutants was also known (Schubert et al, 2018). Moreover, a dechlorination process was observed in non-organohalide-respiring bacteria and under these conditions, the implication of protein-free corrinoids was already suggested (Jagnow et al, 1977;Badea et al, 2009;Lomheim et al, 2020). This last point was confirmed in that study.…”

“…Among these bacteria, Desulfovibrio sp.86 was isolated and showed to degrade chlordecone along with the same TPs profile as observed in presence of Citrobacter sp.86 (Della-Negra et al, 2020). In the same way, in microcosms amended with chlordecone, no known obligate organohalide respiring bacteria were observed, whereas enrichment with Desulfovibrio, Sporomusa, and Geobacter species or methanogens were noticed (Lomheim et al, 2020). Still, in this case, these bacteria and archaea could be corrinoid-producers.…”

Microbial Transformation of Chlordecone and Two Transformation Products Formed During in situ Chemical Reduction

“…In the CLD conditions, a concomitant increase of C 9 Cl 5 H 3 was observed through the increase in the size of the peak area (Figure 1). This degradation pathway with ring opening and dechlorination steps has been well documented for anaerobic microbiological degradation of CLD (Chaussonnerie et al, 2016;Chevallier et al, 2019;Della-Negra et al, 2020;Lomheim et al, 2020).…”

“…However, it should be noted that these experimental results were all obtained under artificial anaerobic conditions, which do not correspond to the real redox state of FWI soils. Additionally, several of these studies (Chevallier et al, 2019;Della-Negra et al, 2020;Lomheim et al, 2020) also highlight the presence of these seven families of transformation products in the West Indian environment, reviving the idea that the microbial biodegradation of CLD under natural conditions remains possible.…”