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Molecular and biochemical biomarkers in the American oyster Crassostrea virginica exposed to herbicide Roundup® at high temperature

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Abstract

Aquatic organisms are frequently exposed to various environmental stressors. Thus, the effects of high temperatures and herbicides on aquatic organisms are a major subject of interest. In this study, we studied the effects of short-term exposure (1 week) to Roundup®, a glyphosate-based herbicide (concentrations: 0.5 and 5 µg/L), on the morphology of gills, digestive glands, and connective tissues, and the expression of heat shock protein-70 (HSP70, a chaperone protein), cytochrome P450 (CYP450, a biomarker of environmental contaminants), dinitrophenyl protein (DNP, a biomarker of protein oxidation), nitrotyrosine protein (NTP, a biomarker of protein nitration), antioxidant enzymes such as superoxidase dismutase (SOD) and catalase (CAT) in tissues of American oyster, Crassostrea virginica (Gmelin, 1791) maintained at high temperature (30 °C). Histological analyses showed an increase in mucous production in the gills and digestive glands, and in hemocyte aggregation in the connective tissues as well as a structural change of lumen in the digestive glands of oysters exposed to Roundup. Immunohistochemical and quantitative RT-PCR analyses showed significant (P < 0.05) increases in HSP70, CYP450, DNP, NTP, CAT, and SOD mRNA and protein expressions in the tissues of oysters exposed to Roundup. Taken together, these results suggest that exposure to Roundup at high temperature induces overproduction of reactive oxygen species/reactive nitrogen species which in turn leads to altered prooxidant-antioxidant activity in oyster tissues. Moreover, our results provide new information on protein oxidation/nitration and antioxidant-dependent mechanisms for HSP70 and CYP450 regulations in oysters exposed to Roundup at high temperature.

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Data availability

All the data generated and analyzed during this study are included in this manuscript and available from the corresponding author upon request.

Abbreviations

CAT:

Catalase

CYP450:

Cytochrome P450

DDT:

Dichlorodiphenyltrichloroethane

DNP:

Dinitrophenyl protein

EP:

Extrapallial

EROD:

Ethoxyresoruffin-o-dietylase

HSP70:

Heat shock protein 70

NTP:

3-Nitrotyrosine protein

PBS:

Phosphate buffer saline

PCB:

Polychlorinated biphenyl

qRT-PCR:

Quantitative real-time polymerase chain reaction

ROS:

Reactive oxygen species

RNS:

Reactive nitrogen species

SOD:

Superoxide dismutase

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Acknowledgements

The authors are grateful to Dr. Drew Davis, School of Earth, Environmental and Marine Sciences, University of Texas Rio Grande Valley (UTRGV), Brownsville, Texas, USA, for critically reviewing and editing the manuscript. We would also like to thank Esmirna Cantu, School of Earth, Environmental and Marine Sciences, UTRGV, for the original drawing of the oyster in the summary figure.

Funding

This study was funded in part by the UTRGV Presidential Graduate Research Assistant (PGRA) to Afsana Chowdhury and a UTRGV SEED grant (grant no. 31050258) to Md Saydur Rahman.

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Authors

Contributions

Md Saydur Rahman provided the research idea and supervised the research. Afsana Chowdhury conducted laboratory studies and collected the data. Afsana Chowdhury and Md Saydur Rahman analyzed the data. Md Saydur Rahman and Afsana Chowdhury designed the figures. Afsana Chowdhury drafted the manuscript. Md Saydur Rahman and Afsana Chowdhury edited and reviewed the manuscript.

Corresponding author

Correspondence to Md Saydur Rahman.

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Ethical approval

Oysters were collected according to the wild-caught species rule and regulations approved by the Texas Parks & Wildlife Department (scientific permit number: SPR-1018–274). The UTRGV Institutional Animal Care and Use Committee do not require an animal use and/or care protocol for research conducted on shellfish. All oysters, however, were cared for and handled following invertebrate standards of Guide for the Care and Use Laboratory Animals in the US National Research Council Committee (https://grants.nih.gov/grants/olaw/guide-for-the-care-and-use-of-laboratory-animals.pdf).

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The authors have approved to submission of the final version of the manuscript.

Conflict of interests

The authors declare that there is no conflict of interest with the contents of this manuscript.

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Responsible Editor: Bruno Nunes

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Chowdhury, A., Rahman, M.S. Molecular and biochemical biomarkers in the American oyster Crassostrea virginica exposed to herbicide Roundup® at high temperature. Environ Sci Pollut Res 30, 94757–94778 (2023). https://doi.org/10.1007/s11356-023-28862-6

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  • DOI: https://doi.org/10.1007/s11356-023-28862-6

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