Evolution of pesticide tolerance and associated changes in the microbiome in the water flea Daphnia magna

Exposure to pesticides can have detrimental effects on aquatic communities of non-target species. Populations can evolve tolerance to pesticides which may rescue them from extinction. However, the evolution of tolerance does not always occur and insights in the underlying mechanisms are scarce. One...

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Main Authors: Lizanne Janssens, Marlies Van de Maele, Vienna Delnat, Charlotte Theys, Shinjini Mukherjee, Luc De Meester, Robby Stoks
Format: Article
Language:English
Published: Elsevier 2022-07-01
Series:Ecotoxicology and Environmental Safety
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S0147651322005371
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author Lizanne Janssens
Marlies Van de Maele
Vienna Delnat
Charlotte Theys
Shinjini Mukherjee
Luc De Meester
Robby Stoks
author_facet Lizanne Janssens
Marlies Van de Maele
Vienna Delnat
Charlotte Theys
Shinjini Mukherjee
Luc De Meester
Robby Stoks
author_sort Lizanne Janssens
collection DOAJ
description Exposure to pesticides can have detrimental effects on aquatic communities of non-target species. Populations can evolve tolerance to pesticides which may rescue them from extinction. However, the evolution of tolerance does not always occur and insights in the underlying mechanisms are scarce. One understudied mechanism to obtain pesticide tolerance in hosts are shifts toward pesticide-degrading bacteria in their microbiome. We carried out experimental evolution trials where replicated experimental populations of the water flea Daphnia magna were exposed to the pesticide chlorpyrifos or a solvent control, after which we performed acute toxicity assays to evaluate the evolution of chlorpyrifos tolerance. Additionally, we quantified changes in the microbiota community composition of whole body and gut samples to assess which sample type best reflected the pesticide tolerance of the Daphnia host. As expected, chlorpyrifos-selected clones became more tolerant to chlorpyrifos as shown by the higher EC50 48 h (36% higher) compared with the control clones. This was associated with shifts in the microbiome composition whereby the abundance of known organophosphate-degrading bacterial genera increased on average ~4 times in the chlorpyrifos-selected clones. Moreover, the abundances of several genera, including the organophosphate-degrading bacteria Pseudomonas, Flavobacterium and Bacillus, were positively correlated with the EC50 48 h of the host populations. These shifts in bacterial genera were similar in magnitude in whole body and gut samples, yet the total abundance of organophosphate-degrading bacteria was ~6 times higher in the whole body samples, suggesting that the gut is not the only body part where pesticide degradation by the microbiome occurs. Our results indicate that the microbiome is an important mediator of the development of tolerance to pesticides in Daphnia.
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spelling doaj.art-bd38817e4eea432f84a2f9711d452ed32022-12-22T02:36:19ZengElsevierEcotoxicology and Environmental Safety0147-65132022-07-01240113697Evolution of pesticide tolerance and associated changes in the microbiome in the water flea Daphnia magnaLizanne Janssens0Marlies Van de Maele1Vienna Delnat2Charlotte Theys3Shinjini Mukherjee4Luc De Meester5Robby Stoks6Evolutionary Stress Ecology and Ecotoxicology, University of Leuven, Debériotstraat 32, 3000 Leuven, BelgiumEvolutionary Stress Ecology and Ecotoxicology, University of Leuven, Debériotstraat 32, 3000 Leuven, BelgiumEvolutionary Stress Ecology and Ecotoxicology, University of Leuven, Debériotstraat 32, 3000 Leuven, BelgiumEvolutionary Stress Ecology and Ecotoxicology, University of Leuven, Debériotstraat 32, 3000 Leuven, BelgiumLaboratory of Reproductive Genomics, University of Leuven, ON I Herestraat 49, 3000 Leuven, BelgiumFreshwater Ecology, Evolution and Biodiversity Conservation, University of Leuven, Debériotstraat 32, 3000 Leuven, Belgium; Leibniz-Institute of Freshwater Ecology and Inland Fisheries, Berlin, Germany; Institute of Biology, Freie Universität Berlin, Berlin, Germany; Berlin-Brandenburg Institute of Advanced Biodiversity Research (BBIB), Berlin, GermanyEvolutionary Stress Ecology and Ecotoxicology, University of Leuven, Debériotstraat 32, 3000 Leuven, Belgium; Corresponding author.Exposure to pesticides can have detrimental effects on aquatic communities of non-target species. Populations can evolve tolerance to pesticides which may rescue them from extinction. However, the evolution of tolerance does not always occur and insights in the underlying mechanisms are scarce. One understudied mechanism to obtain pesticide tolerance in hosts are shifts toward pesticide-degrading bacteria in their microbiome. We carried out experimental evolution trials where replicated experimental populations of the water flea Daphnia magna were exposed to the pesticide chlorpyrifos or a solvent control, after which we performed acute toxicity assays to evaluate the evolution of chlorpyrifos tolerance. Additionally, we quantified changes in the microbiota community composition of whole body and gut samples to assess which sample type best reflected the pesticide tolerance of the Daphnia host. As expected, chlorpyrifos-selected clones became more tolerant to chlorpyrifos as shown by the higher EC50 48 h (36% higher) compared with the control clones. This was associated with shifts in the microbiome composition whereby the abundance of known organophosphate-degrading bacterial genera increased on average ~4 times in the chlorpyrifos-selected clones. Moreover, the abundances of several genera, including the organophosphate-degrading bacteria Pseudomonas, Flavobacterium and Bacillus, were positively correlated with the EC50 48 h of the host populations. These shifts in bacterial genera were similar in magnitude in whole body and gut samples, yet the total abundance of organophosphate-degrading bacteria was ~6 times higher in the whole body samples, suggesting that the gut is not the only body part where pesticide degradation by the microbiome occurs. Our results indicate that the microbiome is an important mediator of the development of tolerance to pesticides in Daphnia.http://www.sciencedirect.com/science/article/pii/S0147651322005371ChlorpyrifosExperimental evolutionMicrobiomeTolerance
spellingShingle Lizanne Janssens
Marlies Van de Maele
Vienna Delnat
Charlotte Theys
Shinjini Mukherjee
Luc De Meester
Robby Stoks
Evolution of pesticide tolerance and associated changes in the microbiome in the water flea Daphnia magna
Ecotoxicology and Environmental Safety
Chlorpyrifos
Experimental evolution
Microbiome
Tolerance
title Evolution of pesticide tolerance and associated changes in the microbiome in the water flea Daphnia magna
title_full Evolution of pesticide tolerance and associated changes in the microbiome in the water flea Daphnia magna
title_fullStr Evolution of pesticide tolerance and associated changes in the microbiome in the water flea Daphnia magna
title_full_unstemmed Evolution of pesticide tolerance and associated changes in the microbiome in the water flea Daphnia magna
title_short Evolution of pesticide tolerance and associated changes in the microbiome in the water flea Daphnia magna
title_sort evolution of pesticide tolerance and associated changes in the microbiome in the water flea daphnia magna
topic Chlorpyrifos
Experimental evolution
Microbiome
Tolerance
url http://www.sciencedirect.com/science/article/pii/S0147651322005371
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