Microbes that Clean Up: Bioremediation of Pesticide-Polluted Banana Fields

The pesticide chlordecone, also known commercially as Kepone® or Curlone®, was globally banned by the Stockholm Convention on Persistent Organic Pollutants in 2009. Mounting evidence suggested that chlordecone is neurotoxic, immunotoxic, hepatotoxic, and spermatotoxic to most living organisms (Multigner et al. 2016). Further, the molecule’s cage structure containing 10 chlorine atoms adsorbs strongly to soil and is poorly water soluble, causing it to persist in the environment. As a result, large areas of the Caribbean, and particularly Guadeloupe, as well as certain parts of Latin America, Africa, and Asia that historically used chlordecone to control banana weevil infestations remain polluted today (Cabidoche et al. 2009). Methods to decontaminate soils are needed to protect the environment, water and food supply. With a project spanning eight years, University of Toronto researchers provide evidence that bioremediation may be a viable approach to decontaminate chlordecone polluted grounds (Lomheim et al. 2020).

In the fall of 2010, Lomheim et al. collected soil and water samples from Guadeloupe to construct batch bottle microcosms to evaluate microbial transformation of chlordecone. These microcosms, which are small simplified closed ecosystems, were kept under strict anaerobic conditions and either poisoned to kill the microbial community or amended periodically with chlordecone and an electron donor (ethanol or acetone) to stimulate dechlorination. While extensive investigation was ongoing to quantify chlordecone decomposition, samples from microcosms were taken and archived periodically over ~3,000 days.

Quantification of chlordecone is challenging due to its strong sorption to soil, low water solubility, and inconsistent ionization for analysis by mass spectrometry. Further, due to high chloride background in the field samples, chloride increase could not be used as a proxy for dechlorination. With insights from prior studies (Moriwaki and Hasegawa 2004; Durimel et al. 2013; Cimetiere et al. 2014), Lomheim et al. developed an LC/MS method to observe chlordecone and metabolites in liquid and soil samples from the microcosms. Their analysis relied on exact masses, unique isotope distribution patterns, and retention times to identify metabolite classes with varying numbers of chlorine substituents. The researchers analyzed nearly 40 microcosms consisting of four treatment groups including active, poisoned, unamended and medium controls and detected 19 different dechlorination products by LC/MS. By eight months, near complete dechlorination was observed in some of the dechlorination products with 9 out of 10 chlorines removed from chlordecone. Overall, the researchers determined that chlordecone was lost to the greatest extent in microbially-active bottles, which also had significantly higher concentrations of metabolites. Additionally, the researchers also calculated and estimated a distribution coefficient from liquid (filtered samples) and soil (soil/water samples). This confirmed the strong sorption of chlordecone to soil and for the first time, provided sorption coefficients for chlordecone metabolites. Interestingly, some metabolites such as the carboxylated intermediates sorb poorly to soil suggesting they could be washed out from soils by rain.

Over the eight years, Lomheim and colleagues monitored the microcosms for anaerobic microbial activity and observed that all non-poisoned microcosms remained active despite the repeated addition of chlordecone. Throughout the study, microcosms were assessed for bacterial abundance using qPCR and community composition using 16S rRNA amplicon sequencing. No clear trends were revealed by these microbial analyses and surprisingly, organohalide respiring bacteria were not consistently identified in any of the chlordecone amended microcosms. Although the team identified other possible facultative dechlorinators such as Anaeromyxobacter and Geobacter in these samples, their presence was generally variable and in low levels. Microbial enrichment will be necessary in future studies to identify the key microbial players in these polluted Guadeloupean soils.

Equipped with their advanced development of an LC/MS method for the detection of chlordecone degradation products, the team returned to the same locations in Guadeloupe to see if metabolites could be detected in fresh field samples. The 2018 field data demonstrated that anaerobic ring opening and dechlorination processes are occurring in situ in Guadeloupe soils.

This work provides evidence that indigenous microorganisms dechlorinated chlordecone in polluted grounds. While the key microbial players have yet to be pinpointed, the researchers suggest open-cage metabolites are more likely to be biodegradable by a wider variety of anaerobic as well as aerobic microbes. This work spanning nearly a decade presents the pioneering evidence for the use of bioremediation to reduce the impact of chlordecone contamination across the globe.

Primary Research Article:

Lomheim, Line, Laurent Laquitaine, Suly Rambinaising, Robert Flick, Andrei Starostine, Corine Jean Marius, Elizabeth A Edwards, and Sarra Gaspard. 2020. “Evidence for Extensive Anaerobic Dechlorination and Transformation of the Pesticide Chlordecone (C10Cl10O) by Indigenous Microbes in Microcosms from Guadeloupe Soil.” PLOS ONE 15 (4): e0231219. https://doi.org/10.1371/journal.pone.0231219.

Other References:

Cabidoche, Y.-M., R Achard, P Cattan, C Clermont-Dauphin, F Massat, and J Sansoulet. 2009. “Long-Term Pollution by Chlordecone of Tropical Volcanic Soils in the French West Indies: A Simple Leaching Model Accounts for Current Residue.” Environmental Pollution 157 (5): 1697–1705. https://doi.org/https://doi.org/10.1016/j.envpol.2008.12.015.

Cimetiere, Nicolas, Sylvain Giraudet, Marie Papazoglou, Hélène Fallou, Abdeltif Amrane, and Pierre Le Cloirec. 2014. “Analysis of Chlordecone by LC/MS–MS in Surface and Wastewaters.” Journal of Environmental Chemical Engineering 2 (2): 849–56. https://doi.org/https://doi.org/10.1016/j.jece.2014.01.010.

Durimel, A, S Altenor, R Miranda-Quintana, P Couespel Du Mesnil, U Jauregui-Haza, R Gadiou, and S Gaspard. 2013. “PH Dependence of Chlordecone Adsorption on Activated Carbons and Role of Adsorbent Physico-Chemical Properties.” Chemical Engineering Journal 229: 239–49. https://doi.org/https://doi.org/10.1016/j.cej.2013.03.036.

Moriwaki, Hiroshi, and Atsuko Hasegawa. 2004. “Detection of Chlordecone by Liquid Chromatography with Tandem Mass Spectrometry.” Rapid Communications in Mass Spectrometry 18 (11): 1243–44. https://doi.org/10.1002/rcm.1474.

Multigner, Luc, Philippe Kadhel, Florence Rouget, Pascal Blanchet, and Sylvaine Cordier. 2016. “Chlordecone Exposure and Adverse Effects in French West Indies Populations.” Environmental Science and Pollution Research 23 (1): 3–8. https://doi.org/10.1007/s11356-015-4621-5.

The Blog Post Author:
Emma LeBlanc
Research Assistant, Cowen Lab

Posted on : 22/06/2020 9:00 AM

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