Multiple stressor effects of insecticide exposure and increased fine sediment deposition on the gene expression profiles of two freshwater invertebrate species

Abstract Background Freshwater ecosystem degradation and biodiversity decline are strongly associated with intensive agricultural practices. Simultaneously occurring agricultural stressors can interact in complex ways, preventing an accurate prediction of their combined effects on aquatic biota. Her...

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Main Authors: Marie V. Brasseur, Dominik Buchner, Leoni Mack, Verena C. Schreiner, Ralf B. Schäfer, Florian Leese, Christoph Mayer
Format: Article
Language:English
Published: SpringerOpen 2023-09-01
Series:Environmental Sciences Europe
Subjects:
Online Access:https://doi.org/10.1186/s12302-023-00785-6
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author Marie V. Brasseur
Dominik Buchner
Leoni Mack
Verena C. Schreiner
Ralf B. Schäfer
Florian Leese
Christoph Mayer
author_facet Marie V. Brasseur
Dominik Buchner
Leoni Mack
Verena C. Schreiner
Ralf B. Schäfer
Florian Leese
Christoph Mayer
author_sort Marie V. Brasseur
collection DOAJ
description Abstract Background Freshwater ecosystem degradation and biodiversity decline are strongly associated with intensive agricultural practices. Simultaneously occurring agricultural stressors can interact in complex ways, preventing an accurate prediction of their combined effects on aquatic biota. Here, we address the limited mechanistic understanding of multiple stressor effects of two globally important stressors, an insecticide (chlorantraniliprole), and increased fine sediment load and assessed their impact on the transcriptomic profile of two stream macroinvertebrates: the amphipod Gammarus pulex and the caddisfly Lepidostoma basale. Results We identified mainly antagonistic stressor interactions at the transcriptional level, presumably because the insecticide adsorbed to fine sediment particles. L. basale, which is phylogenetically more closely related to the insecticide’s target taxon Lepidoptera, exhibited strong transcriptional changes when the insecticide stressor was applied, whereas no clear response patterns were observed in the amphipod G. pulex. These differences in species vulnerability can presumably be attributed to molecular mechanisms determining the cellular affinity toward a stressor as well as differential exposure patterns resulting from varying ecological requirements between L. basale and G. pulex. Interestingly, the transcriptional response induced by insecticide exposure in L. basale was not associated with a disruption of the calcium homeostasis, which is the described mode of action for chlorantraniliprole. Instead, immune responses and alterations of the developmental program appear to play a more significant role. Conclusions Our study shows how transcriptomic data can be used to identify multiple stressor effects and to explore the molecular mechanisms underlying stressor-induced physiological responses. As such, stressor effects assessed at the molecular level can inform about modes of action of chemicals and their interplay with non-chemical stressors. We demonstrated that stressor effects vary between different organismic groups and that insecticide effects are not necessarily covered by their described mode of action, which has important implications for environmental risk assessment of insecticides in non-target organisms.
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spelling doaj.art-8bb897e82627410eb1fccc7daeadaf242023-11-19T12:40:41ZengSpringerOpenEnvironmental Sciences Europe2190-47152023-09-0135111710.1186/s12302-023-00785-6Multiple stressor effects of insecticide exposure and increased fine sediment deposition on the gene expression profiles of two freshwater invertebrate speciesMarie V. Brasseur0Dominik Buchner1Leoni Mack2Verena C. Schreiner3Ralf B. Schäfer4Florian Leese5Christoph Mayer6Centre for Molecular Biodiversity Research, Leibniz Institute for the Analysis of Biodiversity ChangeAquatic Ecosystem Research, University of Duisburg-EssenAquatic Ecology, University of Duisburg-EsseniES Landau, Institute for Environmental Sciences, RPTU Kaiserslautern-LandauiES Landau, Institute for Environmental Sciences, RPTU Kaiserslautern-LandauAquatic Ecosystem Research, University of Duisburg-EssenCentre for Molecular Biodiversity Research, Leibniz Institute for the Analysis of Biodiversity ChangeAbstract Background Freshwater ecosystem degradation and biodiversity decline are strongly associated with intensive agricultural practices. Simultaneously occurring agricultural stressors can interact in complex ways, preventing an accurate prediction of their combined effects on aquatic biota. Here, we address the limited mechanistic understanding of multiple stressor effects of two globally important stressors, an insecticide (chlorantraniliprole), and increased fine sediment load and assessed their impact on the transcriptomic profile of two stream macroinvertebrates: the amphipod Gammarus pulex and the caddisfly Lepidostoma basale. Results We identified mainly antagonistic stressor interactions at the transcriptional level, presumably because the insecticide adsorbed to fine sediment particles. L. basale, which is phylogenetically more closely related to the insecticide’s target taxon Lepidoptera, exhibited strong transcriptional changes when the insecticide stressor was applied, whereas no clear response patterns were observed in the amphipod G. pulex. These differences in species vulnerability can presumably be attributed to molecular mechanisms determining the cellular affinity toward a stressor as well as differential exposure patterns resulting from varying ecological requirements between L. basale and G. pulex. Interestingly, the transcriptional response induced by insecticide exposure in L. basale was not associated with a disruption of the calcium homeostasis, which is the described mode of action for chlorantraniliprole. Instead, immune responses and alterations of the developmental program appear to play a more significant role. Conclusions Our study shows how transcriptomic data can be used to identify multiple stressor effects and to explore the molecular mechanisms underlying stressor-induced physiological responses. As such, stressor effects assessed at the molecular level can inform about modes of action of chemicals and their interplay with non-chemical stressors. We demonstrated that stressor effects vary between different organismic groups and that insecticide effects are not necessarily covered by their described mode of action, which has important implications for environmental risk assessment of insecticides in non-target organisms.https://doi.org/10.1186/s12302-023-00785-6Agricultural stressorAntagonistic interactionChlorantraniliprolePesticideSedimentationSynergistic interaction
spellingShingle Marie V. Brasseur
Dominik Buchner
Leoni Mack
Verena C. Schreiner
Ralf B. Schäfer
Florian Leese
Christoph Mayer
Multiple stressor effects of insecticide exposure and increased fine sediment deposition on the gene expression profiles of two freshwater invertebrate species
Environmental Sciences Europe
Agricultural stressor
Antagonistic interaction
Chlorantraniliprole
Pesticide
Sedimentation
Synergistic interaction
title Multiple stressor effects of insecticide exposure and increased fine sediment deposition on the gene expression profiles of two freshwater invertebrate species
title_full Multiple stressor effects of insecticide exposure and increased fine sediment deposition on the gene expression profiles of two freshwater invertebrate species
title_fullStr Multiple stressor effects of insecticide exposure and increased fine sediment deposition on the gene expression profiles of two freshwater invertebrate species
title_full_unstemmed Multiple stressor effects of insecticide exposure and increased fine sediment deposition on the gene expression profiles of two freshwater invertebrate species
title_short Multiple stressor effects of insecticide exposure and increased fine sediment deposition on the gene expression profiles of two freshwater invertebrate species
title_sort multiple stressor effects of insecticide exposure and increased fine sediment deposition on the gene expression profiles of two freshwater invertebrate species
topic Agricultural stressor
Antagonistic interaction
Chlorantraniliprole
Pesticide
Sedimentation
Synergistic interaction
url https://doi.org/10.1186/s12302-023-00785-6
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