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Transcriptional and biochemical biomarker responses in a freshwater mussel (Anodonta anatina) under environmentally relevant Cu exposure
University of Skövde, School of Bioscience. University of Skövde, Systems Biology Research Environment. Department of Biology, Lund University, Sweden. (Ekologisk modellering, Ecological Modeling)ORCID iD: 0000-0002-2418-1163
University of Skövde, School of Bioscience. University of Skövde, Systems Biology Research Environment. (Ekologisk modellering, Ecological Modeling)ORCID iD: 0000-0002-3965-7371
University of Skövde, School of Bioscience. University of Skövde, Systems Biology Research Environment. (Translationell bioinformatik, Translational Bioinformatics)ORCID iD: 0000-0001-6254-4335
TATAA Biocenter, Gothenburg, Sweden.
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2020 (English)In: Environmental Science and Pollution Research, ISSN 0944-1344, E-ISSN 1614-7499, Vol. 27, no 9, p. 9999-10010Article in journal (Refereed) Published
Abstract [en]

Molecular biomarkers, like gene transcripts or enzyme activities, are potentially powerful tools for early warning assessment of pollution. However, a thorough understanding of response and baseline variation is required to distinguish actual effects from pollution. Here, we assess the freshwater mussel Anodonta anatina as a biomarker model species for freshwater ecosystems, by testing responses of six transcriptional (cat, gst, hsp70, hsp90, mt, and sod) and two biochemical (AChE and GST) biomarkers to environmentally relevant Cu water concentrations. Mussels (n = 20), collected from a stream free from point source pollution, were exposed in the laboratory, for 96 h, to Cu treatments (< 0.2 mu g/L, 0.77 +/- 0.87 mu g/L, and 6.3 +/- 5.4 mu g/L). Gills and digestive glands were extracted and analyzed for transcriptional and biochemical responses. Biological and statistical effect sizes from Cu treatments were in general small (mean log(2) fold-change <= 0.80 and Cohen's f <= 0.69, respectively), and no significant treatment effects were observed. In contrast, four out of eight biomarkers (cat, gst, hsp70, and GST) showed a significant sex:tissue interaction, and additionally one (sod) showed significant overall effects from sex. Specifically, three markers in gills (cat, mt, GST) and one in digestive gland (AChE) displayed significant sex differences, independent of treatment. Results suggest that sex or tissue effects might obscure low-magnitude biomarker responses and potential early warnings. Thus, variation in biomarker baselines and response patterns needs to be further addressed for the future use of A. anatina as a biomarker model species.

Place, publisher, year, edition, pages
Springer Berlin/Heidelberg, 2020. Vol. 27, no 9, p. 9999-10010
Keywords [en]
Bivalve, Gene expression, Response variability, Sex effects, Effect size, RT-qPCR
National Category
Other Biological Topics
Research subject
INF502 Biomarkers; Ecological Modelling Group; Bioinformatics
Identifiers
URN: urn:nbn:se:his:diva-18132DOI: 10.1007/s11356-020-07660-4ISI: 000524949600099PubMedID: 31933076Scopus ID: 2-s2.0-85077999744OAI: oai:DiVA.org:his-18132DiVA, id: diva2:1385563
Funder
Knowledge Foundation
Note

CC BY 4.0

Environmental Science and Pollution Research. ISSN: 0944-1344 (Print) 1614-7499 (Online)

Available from: 2020-01-14 Created: 2020-01-14 Last updated: 2023-01-12Bibliographically approved
In thesis
1. Transcriptional biomarkers of toxicity – powerful tools or random noise?: An applied perspective from studies on bivalves
Open this publication in new window or tab >>Transcriptional biomarkers of toxicity – powerful tools or random noise?: An applied perspective from studies on bivalves
2023 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

Aquatic organisms are constantly at risk of being exposed to potentially harmful chemical compounds of natural or anthropogenic origin. Biological life can for instance respond to chemical stressors by changes in gene expression, and thus, certain gene transcripts can potentially function as biomarkers, i.e. early warnings, of toxicity and chemical stress. A major challenge for biomarker application is the extrapolation of transcriptional data to potential effects at the organism level or above. Importantly, successful biomarker use also requires basal understanding of how to distinguish actual responses from background noise. The aim of this thesis is, based on response magnitude and variation, to evaluate the biomarker potential in a set of putative transcriptional biomarkers of general toxicity and chemical stress.

Specifically, I addressed a selection of six transcripts involved in cytoprotection and oxidative stress: catalase (cat), glutathione-S-transferase (gst), heat shock proteins 70 and 90 (hsp70, hsp90), metallothionein (mt) and superoxide dismutase (sod). Moreover, I used metal exposures to serve as a proxy for general chemical stress, and due to their ecological relevance and nature as sedentary filter-feeders, I used bivalves as study organisms.

In a series of experiments, I tested transcriptional responses in the freshwater duck mussel, Anodonta anatina, exposed to copper or an industrial wastewater effluent, to address response robustness and sensitivity, and potential controlled (e.g. exposure concentration) and random (e.g. gravidness) sources of variation. In addition, I performed a systematic review and meta-analysis on transcriptional responses in metal exposed bivalves to (1) evaluate what responses to expect from arbitrary metal exposures, (2) assess the influence from metal concentration (expressed as toxic unit), exposure time and analyzed tissue, and (3) address potential impacts from publication bias in the scientific literature.

Response magnitudes were generally small in relationship to the observed variation, both for A. anatina and bivalves in general. The expected response to an arbitrary metal exposure would generally be close to zero, based on both experimental observations and on the estimated impact from publication bias. Although many of the transcripts demonstrated concentration-response relationships, large background noise might in practice obscure the small responses even at relatively high exposures. As demonstrated in A. anatina under copper exposure, this can be the case already for single species under high resolution exposures to single pollutants. As demonstrated by the meta-regression, this problem can only be expected to increase further upon extrapolation between different species and exposure scenarios, due to increasing heterogeneity and random variation. Similar patterns can also be expected for time-dependent response variation, although the meta-regression revealed a general trend of slightly increasing response magnitude with increasing exposure times.

In A. anatina, gravidness was identified as a source of random variability that can potentially affect the baseline of most assessed biomarkers, particularly when quantified in gills. Response magnitudes and variability in this species were generally similar for selected transcripts as for two biochemical biomarkers included for comparison (AChE, GST), suggesting that the transcripts might not capture early warnings more efficiently than other molecular endpoints that are more toxicologically relevant. Overall, high concentrations and long exposure durations presumably increase the likelihood of a detectable transcriptional response, but not to an extent that justifies universal application as biomarkers of general toxicity and chemical stress. Consequently, without a strictly defined and validated application, this approach on its own appears unlikely to be successful for future environmental risk assessment and monitoring. Ultimately, efficient use of transcriptional biomarkers might require additional implementation of complementary approaches offered by current molecular techniques.

Place, publisher, year, edition, pages
Lund: Lund University (Media-Tryck), 2023. p. 199
Keywords
Biomarkers, Bivalves, Bivalvia, Ecotoxicology, Environmental toxicology, Environmental risk assessment, RT-qPCR, qPCR, Quantitative PCR, Systematic review, Meta-analysis, Dose-response relationships, Concentration-response relationships, Heavy metals, Metals, General toxicity, Copper, Duck mussel, Anodonta anatina, Freshwater, Gene transcription, Biomarkörer, Musslor, Bivalvia, Ekotoxikologi, Miljötoxikologi, Miljöriskbedömning, RT-qPCR, qPCR, Kvantitativ PCR, Systematic review, Metaanalys, Dos-responssamband, Koncentration-responssamband, Tungmetaller, Metaller, Allmän toxicitet, Koppar, Allmän dammussla, Anodonta anatina, Sötvatten, Gentranskription
National Category
Biochemistry and Molecular Biology Pharmacology and Toxicology Environmental Sciences Genetics and Genomics Ecology
Research subject
Ecological Modelling Group
Identifiers
urn:nbn:se:his:diva-22180 (URN)978-91-8039-496-3 (ISBN)978-91-8039-495-6 (ISBN)
Public defence
2023-02-10, Blå hallen, Sölvegatan 37, Lund, 09:00 (English)
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Supervisors
Available from: 2023-01-12 Created: 2023-01-12 Last updated: 2025-02-01Bibliographically approved

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Ekelund Ugge, Gustaf Magnus OskarJonsson, AnnieOlsson, Björn

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