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Evidence for extensive anaerobic dechlorination and transformation of the pesticide chlordecone (C(10)Cl(10)O) by indigenous microbes in microcosms from Guadeloupe soil

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 bis-homocubane structure is...

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Autores principales: Lomheim, Line, Laquitaine, Laurent, Rambinaising, Suly, Flick, Robert, Starostine, Andrei, Jean-Marius, Corine, Edwards, Elizabeth A., Gaspard, Sarra
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7153859/
https://www.ncbi.nlm.nih.gov/pubmed/32282845
http://dx.doi.org/10.1371/journal.pone.0231219
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author Lomheim, Line
Laquitaine, Laurent
Rambinaising, Suly
Flick, Robert
Starostine, Andrei
Jean-Marius, Corine
Edwards, Elizabeth A.
Gaspard, Sarra
author_facet Lomheim, Line
Laquitaine, Laurent
Rambinaising, Suly
Flick, Robert
Starostine, Andrei
Jean-Marius, Corine
Edwards, Elizabeth A.
Gaspard, Sarra
author_sort Lomheim, Line
collection PubMed
description 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 bis-homocubane 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 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.
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spelling pubmed-71538592020-04-16 Evidence for extensive anaerobic dechlorination and transformation of the pesticide chlordecone (C(10)Cl(10)O) by indigenous microbes in microcosms from Guadeloupe soil Lomheim, Line Laquitaine, Laurent Rambinaising, Suly Flick, Robert Starostine, Andrei Jean-Marius, Corine Edwards, Elizabeth A. Gaspard, Sarra PLoS One Research Article 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 bis-homocubane 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 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. Public Library of Science 2020-04-13 /pmc/articles/PMC7153859/ /pubmed/32282845 http://dx.doi.org/10.1371/journal.pone.0231219 Text en © 2020 Lomheim et al http://creativecommons.org/licenses/by/4.0/ This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Lomheim, Line
Laquitaine, Laurent
Rambinaising, Suly
Flick, Robert
Starostine, Andrei
Jean-Marius, Corine
Edwards, Elizabeth A.
Gaspard, Sarra
Evidence for extensive anaerobic dechlorination and transformation of the pesticide chlordecone (C(10)Cl(10)O) by indigenous microbes in microcosms from Guadeloupe soil
title Evidence for extensive anaerobic dechlorination and transformation of the pesticide chlordecone (C(10)Cl(10)O) by indigenous microbes in microcosms from Guadeloupe soil
title_full Evidence for extensive anaerobic dechlorination and transformation of the pesticide chlordecone (C(10)Cl(10)O) by indigenous microbes in microcosms from Guadeloupe soil
title_fullStr Evidence for extensive anaerobic dechlorination and transformation of the pesticide chlordecone (C(10)Cl(10)O) by indigenous microbes in microcosms from Guadeloupe soil
title_full_unstemmed Evidence for extensive anaerobic dechlorination and transformation of the pesticide chlordecone (C(10)Cl(10)O) by indigenous microbes in microcosms from Guadeloupe soil
title_short Evidence for extensive anaerobic dechlorination and transformation of the pesticide chlordecone (C(10)Cl(10)O) by indigenous microbes in microcosms from Guadeloupe soil
title_sort evidence for extensive anaerobic dechlorination and transformation of the pesticide chlordecone (c(10)cl(10)o) by indigenous microbes in microcosms from guadeloupe soil
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7153859/
https://www.ncbi.nlm.nih.gov/pubmed/32282845
http://dx.doi.org/10.1371/journal.pone.0231219
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