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

• Published in: PloS one 2020-04, Vol.15 (4), p.e0231219
• Main Authors: Lomheim, Line, Laquitaine, Laurent, Rambinaising, Suly, Flick, Robert, Starostine, Andrei, Jean-Marius, Corine, Edwards, Elizabeth A, Gaspard, Sarra
• Format: Article
• Language: English
• Subjects: Acetone; Aerobic conditions; Ammonia; Anaerobic microorganisms; Anaerobic processes; Attenuation; Biological activity; Biology and Life Sciences; Bioremediation; Biotransformation; Cages; Chemical engineering; Chemistry; Chlordecone; Chlorine; Dechlorination; Degradation products; Derivatives; Earth Sciences; Ecology and Environmental Sciences; Ethanol; Intermediates; Laboratories; Land pollution; Metabolites; Methods; Microcosms; Microorganisms; Natural attenuation; NMR; Nuclear magnetic resonance; Pesticides; Physical Sciences; Researchers; Sediment pollution; Sludge; Soil analysis; Soil contamination; Soil pollution; Soil water; Soils; Transformations; Vitamin B12; Water pollution
• ISSN: 1932-6203; 1932-6203
• DOI: 10.1371/journal.pone.0231219

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