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...
Main Authors: | , , , , , , |
---|---|
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 |
_version_ | 1811337725211574272 |
---|---|
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. |
first_indexed | 2024-04-13T17:59:03Z |
format | Article |
id | doaj.art-bd38817e4eea432f84a2f9711d452ed3 |
institution | Directory Open Access Journal |
issn | 0147-6513 |
language | English |
last_indexed | 2024-04-13T17:59:03Z |
publishDate | 2022-07-01 |
publisher | Elsevier |
record_format | Article |
series | Ecotoxicology and Environmental Safety |
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 |
work_keys_str_mv | AT lizannejanssens evolutionofpesticidetoleranceandassociatedchangesinthemicrobiomeinthewaterfleadaphniamagna AT marliesvandemaele evolutionofpesticidetoleranceandassociatedchangesinthemicrobiomeinthewaterfleadaphniamagna AT viennadelnat evolutionofpesticidetoleranceandassociatedchangesinthemicrobiomeinthewaterfleadaphniamagna AT charlottetheys evolutionofpesticidetoleranceandassociatedchangesinthemicrobiomeinthewaterfleadaphniamagna AT shinjinimukherjee evolutionofpesticidetoleranceandassociatedchangesinthemicrobiomeinthewaterfleadaphniamagna AT lucdemeester evolutionofpesticidetoleranceandassociatedchangesinthemicrobiomeinthewaterfleadaphniamagna AT robbystoks evolutionofpesticidetoleranceandassociatedchangesinthemicrobiomeinthewaterfleadaphniamagna |