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. 2023 Jul 1:880:163269.
doi: 10.1016/j.scitotenv.2023.163269. Epub 2023 Apr 5.

Exposure of adult zebrafish (Danio rerio) to SARS-CoV-2 at predicted environmentally relevant concentrations: Outspreading warns about ecotoxicological risks to freshwater fish

Thiarlen Marinho da Luz  1 , Abraão Tiago Batista Guimarães  2 , Stênio Gonçalves da Silva Matos  2 , Sindoval Silva de Souza  3 , Alex Rodrigues Gomes  4 , Aline Sueli de Lima Rodrigues  1 , Edison Luiz Durigon  5 , Ives Charlie-Silva  6 , Ítalo Nascimento Freitas  4 , Abu Reza Md Towfiqul Islam  7 , Md Mostafizur Rahman  8 , Abner Marcelino Silva  2 , Guilherme Malafaia  9
Affiliations

Exposure of adult zebrafish (Danio rerio) to SARS-CoV-2 at predicted environmentally relevant concentrations: Outspreading warns about ecotoxicological risks to freshwater fish

Thiarlen Marinho da Luz et al. Sci Total Environ. .

Retraction in

Abstract

While the multifaceted social, economic, and public health impacts associated with the COVID-19 pandemic are known, little is known about its effects on non-target aquatic ecosystems and organisms. Thus, we aimed to evaluate the potential ecotoxicity of SARS-CoV-2 lysate protein (SARS.CoV2/SP02.2020.HIAE.Br) in adult zebrafish (Danio rerio) at predicted environmentally relevant concentrations (0.742 and 2.226 pg/L), by 30 days. Although our data did not show locomotor alterations or anxiety-like or/and anxiolytic-like behavior, we noticed that exposure to SARS-CoV-2 negatively affected habituation memory and social aggregation of animals in response to a potential aquatic predator (Geophagus brasiliensis). An increased frequency of erythrocyte nuclear abnormalities was also observed in animals exposed to SARS-CoV-2. Furthermore, our data suggest that such changes were associated with a redox imbalance [↑ROS (reactive oxygen species), ↑H2O2 (hydrogen peroxide), ↓SOD (superoxide dismutase), and ↓CAT (catalase)], cholinesterasic effect [↑AChE (acetylcholinesterase) activity], as well as the induction of an inflammatory immune response [↑NO (nitric oxide), ↑IFN-γ (interferon-gamma), and ↓IL-10 (interleukin-10)]. For some biomarkers, we noticed that the response of the animals to the treatments was not concentration-dependent. However, principal component analysis (PCA) and the "Integrated Biomarker Response" index (IBRv2) indicated a more prominent ecotoxicity of SARS-CoV-2 at 2.226 pg/L. Therefore, our study advances knowledge about the ecotoxicological potential of SARS-CoV-2 and reinforces the presumption that the COVID-19 pandemic has negative implications beyond its economic, social, and public health impacts.

Keywords: Biomarkers; Danio rerio; Ecotoxicity; Environmental toxicology; New coronavirus.

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Conflict of interest statement

Declaration of competing interest We confirm that there are no known conflicts of interest associated with this work, and there has been no significant financial support for this work that could have influenced its outcome. Furthermore, we ensure that the manuscript has been read and approved by all named authors and that there are no other persons who satisfied the criteria for authorship but are not listed. We further confirm that all have approved the order of authors listed in the manuscript of us. Due care has been taken to ensure the integrity of the work.

Figures

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Graphical abstract
Fig. 1
Fig. 1
(A–B) Total crossings at different times of the open field test of adult zebrafish (Danio rerio) unexposed or exposed to SARS-CoV-2 at different concentrations. In “A”, the correlation and linear regression analyses' statistical summaries are presented next to the graph. In “B”, non-parametric data are displayed by the median and interquartile range, and statistical summaries are shown alongside the graph. Distinct lowercase letters indicate significant differences. SARS-I and SARS-II: composite groups of zebrafish exposed to SARS-CoV-2 lysate protein at 0.742 and 2.226 pg/L, respectively.
Fig. 2
Fig. 2
Cluster index of zebrafish shoals (Danio rerio) unexposed or exposed to SARS-CoV-2 at different concentrations in the social aggregation test in response to a potential aquatic predator (Geophagus brasiliensis). Non-parametric data are displayed by the median and interquartile range, and statistical summaries are displayed at the top of the graph. Distinct lowercase letters indicate significant differences. SARS-I and SARS-II: composite groups of zebrafish exposed to SARS-CoV-2 lysate protein at 0.742 and 2.226 pg/L, respectively. WP: without predatory stimulation and P: with predatory stimulus.
Fig. 3
Fig. 3
(A–B) Reactive oxygen species (ROS) production, (C–D) hydrogen peroxide levels (H2O2), (E–F) superoxide dismutase, and (G-H) catalase activity in adult zebrafish (Danio rerio) unexposed or exposed to SARS-CoV-2 at different concentrations. In “A”, “C”, “E”, and “G”, parametric data are presented by the mean + standard deviation, whereas non-parametric data are presented by the median and interquartile range. Distinct lowercase letters indicate significant differences. Statistical summaries are shown next to the graphs. SARS-I and SARS-II: composite groups of zebrafish exposed to SARS-CoV-2 lysate protein at 0.742 and 2.226 pg/L, respectively.
Fig. 4
Fig. 4
(A–B) Acetylcholinesterase activity in adult zebrafish (Danio rerio) unexposed or exposed to SARS-CoV-2 at different concentrations. In “A”, non-parametric data are presented by the median and interquartile range. Distinct lowercase letters indicate significant differences. Statistical summaries are shown next to the graphs. SARS-I and SARS-II: composite groups of zebrafish exposed to SARS-CoV-2 lysate protein at 0.742 and 2.226 pg/L, respectively.
Fig. 5
Fig. 5
(A–B) Nitrite production, (C) interleukin 10 (IL-10), and (D) interferon γ (IFN-γ) levels in adult zebrafish (Danio rerio) unexposed or exposed to SARS-CoV-2 at different concentrations. In “A”, “C”, and “D”, parametric data are presented by the mean + standard deviation. Distinct lowercase letters indicate significant differences. Statistical summaries are shown next to the graphs. SARS-I and SARS-II: composite groups of zebrafish exposed to SARS-CoV-2 lysate protein at 0.742 and 2.226 pg/L, respectively.
Fig. 6
Fig. 6
(A–B) Total nuclear abnormalities in erythrocytes and (C) frequency of different types of abnormalities evidenced in adult zebrafish (Danio rerio) unexposed or exposed to SARS-CoV-2 at different concentrations. In “A” and “C”, parametric data are presented by the mean + standard deviation, whereas non-parametric data are presented by the median and interquartile range. Distinct lowercase letters indicate significant differences. Statistical summaries are shown next to the graphs. SARS-I and SARS-II: composite groups of zebrafish exposed to SARS-CoV-2 lysate protein at 0.742 and 2.226 pg/L, respectively.
Fig. 7
Fig. 7
(A) Loadings plot of the investigated variables, (B) PC score plot, and (C) PCA biplot of the first two principal components (PCs) that simultaneously shows scores of experimental groups. See the meanings of the acronyms in Table S1. In “C”, the blue arrows point to the PC2 Scores of the experimental groups. SARS-I and SARS-II: composite groups of zebrafish exposed to SARS-CoV-2 lysate protein at 0,742 and 2.226 pg/L, respectively.
Fig. 8
Fig. 8
(A) “Integrated Biomarker Response” index (IBRv2) calculated for groups composed of adult zebrafish (Danio rerio) unexposed or exposed to SARS-CoV-2 at different concentrations. (B and C): A-values derived from the IBRv2 obtained for the respective groups exposed to the SARS-CoV-2. SARS-I and SARS-II: composite groups of zebrafish exposed to SARS-CoV-2 lysate protein at 0.742 and 2.226 pg/L, respectively. See the meanings of the acronyms in Table S1.
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