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Response of digestive enzymes and esterases of ecotoxicological concern in earthworms exposed to chlorpyrifos-treated soils

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Abstract

Assessment of organophosphorus (OP) pesticide exposure in non-target organisms rarely involves non-neural molecular targets. Here we performed a 30-d microcosm experiment with Lumbricus terrestris to determine whether the activity of digestive enzymes (phosphatase, β-glucosidase, carboxylesterase and lipase) was sensitive to chlorpyrifos (5 mg kg−1 wet soil). Likewise, acetylcholinesterase (AChE) and butyrylcholinesterase (BChE) activities were measured in the wall muscle and gastrointestinal tissues as indicators of OP exposure. Chlorpyrifos inhibited the acid phosphatase (34% of controls), carboxylesterase (25.6%) and lipase activities (31%) in the gastrointestinal content. However, in the gastrointestinal tissue, only the carboxylesterase and lipase activities were significantly depressed (42–67% carboxylesterase inhibition in the foregut and crop/gizzard, and 15% lipase inhibition in the foregut). Chlorpyrifos inhibited the activity of both cholinesterases in the gastrointestinal tissues, whereas the AChE activity was affected in the wall muscle. These results suggested chlorpyrifos was widely distributed throughout the earthworm body after 30 d of incubation. Interestingly, we found muscle carboxylesterase activity strongly inhibited (92% of control) compared with that detected in the gastrointestinal tissues of the same OP-exposed individuals. This finding was explained by the occurrence of pesticide-resistant esterases in the gastrointestinal tissues, which were evidenced by zymography. Our results suggest that digestive processes of L. terrestris may be altered by chlorpyrifos, as a consequence of the inhibitory action of the insecticide on some digestive enzymes.

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Acknowledgements

We thank the regional Goverment Junta de Comunidades de Castilla-La Mancha (grant no. PEII-2014-001-P) and the Ministerio de Economía y Competitividad (grant no. CTM2014-53915-R) and for their financial support of this research. JM Ríos and AM Attademo thank to Vicerrectorado de Investigación of University Castilla-La Mancha for funding grants as visiting researchers. The comments of two anonymous reviewers were greatly appreciated and contributed to improve this manuscript.

Funding

This study was funded by the regional Government Junta de Comunidades de Castilla-La Mancha (grant no. PEII-2014-001-P) and the Spanish Ministerio de Economía y Competitividad (grant no. CTM2014-53915-R).

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Authors and Affiliations

  1. Laboratory of Ecotoxicology, Faculty of Environmental Science and Biochemistry, University of Castilla-La Mancha, 45071, Toledo, Spain

    Juan C. Sanchez-Hernandez

  2. Laboratorio de Química Ambiental, Instituto Argentino de Nivología, Glaciología y Ciencias Ambientales (IANIGLA)-CONICET, P.O. Box 131, ZC5500, Mendoza, Argentina

    Juan Manuel Ríos

  3. Laboratorio de Ecotoxicología, Facultad de Bioquímica y Ciencias Biológicas, Universidad Nacional del Litoral (FBCB-UNL-CONICET), Paraje El Pozo s/n, 3000, Santa Fe, Argentina

    Andrés M. Attademo

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Correspondence to Juan C. Sanchez-Hernandez.

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This article does not contain any studies with human participants or animals performed by any of the authors, according to the Directive 2010/63/EU of the European Parliament and of the Council of 22 September 2010 on the protection of animals used for scientific purposes (Official Journal of the European Union L 276/33, 20-10-2010).

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Sanchez-Hernandez, J.C., Ríos, J.M. & Attademo, A.M. Response of digestive enzymes and esterases of ecotoxicological concern in earthworms exposed to chlorpyrifos-treated soils. Ecotoxicology 27, 890–899 (2018). https://doi.org/10.1007/s10646-018-1914-8

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