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Impacts of multiple anthropogenic stressors on the transcriptional response of Gammarus fossarum in a mesocosm field experiment

Brasseur, Marie V. ; Beermann, Arne J. ; Elbrecht, Vasco ; Grabner, Daniel ; Peinert-Voss, Bianca ; Salis, Romana LU orcid ; Weiss, Martina ; Mayer, Christoph and Leese, Florian (2022) In BMC Genomics 23.
Abstract

Background: Freshwaters are exposed to multiple anthropogenic stressors, leading to habitat degradation and biodiversity decline. In particular, agricultural stressors are known to result in decreased abundances and community shifts towards more tolerant taxa. However, the combined effects of stressors are difficult to predict as they can interact in complex ways, leading to enhanced (synergistic) or decreased (antagonistic) response patterns. Furthermore, stress responses may remain undetected if only the abundance changes in ecological experiments are considered, as organisms may have physiological protective pathways to counteract stressor effects. Therefore, we here used transcriptome-wide sequencing data to quantify single and... (More)

Background: Freshwaters are exposed to multiple anthropogenic stressors, leading to habitat degradation and biodiversity decline. In particular, agricultural stressors are known to result in decreased abundances and community shifts towards more tolerant taxa. However, the combined effects of stressors are difficult to predict as they can interact in complex ways, leading to enhanced (synergistic) or decreased (antagonistic) response patterns. Furthermore, stress responses may remain undetected if only the abundance changes in ecological experiments are considered, as organisms may have physiological protective pathways to counteract stressor effects. Therefore, we here used transcriptome-wide sequencing data to quantify single and combined effects of elevated fine sediment deposition, increased salinity and reduced flow velocity on the gene expression of the amphipod Gammarus fossarum in a mesocosm field experiment. Results: Stressor exposure resulted in a strong transcriptional suppression of genes involved in metabolic and energy consuming cellular processes, indicating that G. fossarum responds to stressor exposure by directing energy to vitally essential processes. Treatments involving increased salinity induced by far the strongest transcriptional response, contrasting the observed abundance patterns where no effect was detected. Specifically, increased salinity induced the expression of detoxification enzymes and ion transporter genes, which control the membrane permeability of sodium, potassium or chloride. Stressor interactions at the physiological level were mainly antagonistic, such as the combined effect of increased fine sediment and reduced flow velocity. The compensation of the fine sediment induced effect by reduced flow velocity is in line with observations based on specimen abundance data. Conclusions: Our findings show that gene expression data provide new mechanistic insights in responses of freshwater organisms to multiple anthropogenic stressors. The assessment of stressor effects at the transcriptomic level and its integration with stressor effects at the level of specimen abundances significantly contribute to our understanding of multiple stressor effects in freshwater ecosystems.

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author
; ; ; ; ; ; ; and
publishing date
type
Contribution to journal
publication status
published
keywords
Antagonistic stressor interaction, Flow alteration, Gene expression, Metabolic depression, Salinisation, Sedimentation, Transcriptomic stress
in
BMC Genomics
volume
23
article number
816
pages
12 pages
publisher
BioMed Central (BMC)
external identifiers
  • pmid:36482300
  • scopus:85143561377
ISSN
1471-2164
DOI
10.1186/s12864-022-09050-1
language
English
LU publication?
no
additional info
Funding Information: Open Access funding enabled and organized by Projekt DEAL. The experimental field work was performed as part of the GeneStream project of FL, funded by the Kurt Eberhard Bode Foundation (Stifterverband für die Deutsche Wissenschaft). RNA-seq was supported by a grant of the Center of Aquatic and Environmental Research (ZWU) to DG and AB. MVB was supported by a grant of the Deutsche Forschungsgemeinschaft (DFG, MA 3684/3–1). RS was partly supported by DFG grant LE 2323/7–1. Publisher Copyright: © 2022, The Author(s).
id
08824f33-03a0-4621-bca7-6c953a0f6d84
date added to LUP
2023-03-17 10:09:17
date last changed
2024-04-18 10:09:09
@article{08824f33-03a0-4621-bca7-6c953a0f6d84,
  abstract     = {{<p>Background: Freshwaters are exposed to multiple anthropogenic stressors, leading to habitat degradation and biodiversity decline. In particular, agricultural stressors are known to result in decreased abundances and community shifts towards more tolerant taxa. However, the combined effects of stressors are difficult to predict as they can interact in complex ways, leading to enhanced (synergistic) or decreased (antagonistic) response patterns. Furthermore, stress responses may remain undetected if only the abundance changes in ecological experiments are considered, as organisms may have physiological protective pathways to counteract stressor effects. Therefore, we here used transcriptome-wide sequencing data to quantify single and combined effects of elevated fine sediment deposition, increased salinity and reduced flow velocity on the gene expression of the amphipod Gammarus fossarum in a mesocosm field experiment. Results: Stressor exposure resulted in a strong transcriptional suppression of genes involved in metabolic and energy consuming cellular processes, indicating that G. fossarum responds to stressor exposure by directing energy to vitally essential processes. Treatments involving increased salinity induced by far the strongest transcriptional response, contrasting the observed abundance patterns where no effect was detected. Specifically, increased salinity induced the expression of detoxification enzymes and ion transporter genes, which control the membrane permeability of sodium, potassium or chloride. Stressor interactions at the physiological level were mainly antagonistic, such as the combined effect of increased fine sediment and reduced flow velocity. The compensation of the fine sediment induced effect by reduced flow velocity is in line with observations based on specimen abundance data. Conclusions: Our findings show that gene expression data provide new mechanistic insights in responses of freshwater organisms to multiple anthropogenic stressors. The assessment of stressor effects at the transcriptomic level and its integration with stressor effects at the level of specimen abundances significantly contribute to our understanding of multiple stressor effects in freshwater ecosystems.</p>}},
  author       = {{Brasseur, Marie V. and Beermann, Arne J. and Elbrecht, Vasco and Grabner, Daniel and Peinert-Voss, Bianca and Salis, Romana and Weiss, Martina and Mayer, Christoph and Leese, Florian}},
  issn         = {{1471-2164}},
  keywords     = {{Antagonistic stressor interaction; Flow alteration; Gene expression; Metabolic depression; Salinisation; Sedimentation; Transcriptomic stress}},
  language     = {{eng}},
  publisher    = {{BioMed Central (BMC)}},
  series       = {{BMC Genomics}},
  title        = {{Impacts of multiple anthropogenic stressors on the transcriptional response of Gammarus fossarum in a mesocosm field experiment}},
  url          = {{http://dx.doi.org/10.1186/s12864-022-09050-1}},
  doi          = {{10.1186/s12864-022-09050-1}},
  volume       = {{23}},
  year         = {{2022}},
}