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Multiple effects of a commercial Roundup® formulation on the soil filamentous fungus Aspergillus nidulans at low doses: evidence of an unexpected impact on energetic metabolism

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Abstract

Soil microorganisms are highly exposed to glyphosate-based herbicides (GBH), especially to Roundup® which is widely used worldwide. However, studies on the effects of GBH formulations on specific non-rhizosphere soil microbial species are scarce. We evaluated the toxicity of a commercial formulation of Roundup® (R450), containing 450 g/L of glyphosate (GLY), on the soil filamentous fungus Aspergillus nidulans, an experimental model microorganism. The median lethal dose (LD50) on solid media was between 90 and 112 mg/L GLY (among adjuvants, which are also included in the Roundup® formulation), which corresponds to a dilution percentage about 100 times lower than that used in agriculture. The LOAEL and NOAEL (lowest- and no-observed-adverse-effect levels) associated to morphology and growth were 33.75 and 31.5 mg/L GLY among adjuvants, respectively. The formulation R450 proved to be much more active than technical GLY. At the LD50 and lower concentrations, R450 impaired growth, cellular polarity, endocytosis, and mitochondria (average number, total volume and metabolism). In contrast with the depletion of mitochondrial activities reported in animal studies, R450 caused a stimulation of mitochondrial enzyme activities, thus revealing a different mode of action of Roundup® on energetic metabolism. These mitochondrial disruptions were also evident at a low dose corresponding to the NOAEL for macroscopic parameters, indicating that these mitochondrial biomarkers are more sensitive than those for growth and morphological ones. Altogether, our data indicate that GBH toxic effects on soil filamentous fungi, and thus potential impairment of soil ecosystems, may occur at doses far below recommended agricultural application rate.

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Acknowledgments

This work was supported by the University Paris-Sud (UPSud), the Risk Pole from the University of Caen, the non-governmental organization “Générations Futures” and the Committee for Independent Research and Information on Genetic Engineering (CRIIGEN). It received funding from the Regional Council Ile-de-France and the UPSud. We thank Soraya Hadi for technical assistance. We are grateful to Professor J.-P. Bourdineaud and Dr. R. Mesnage for proofreading the article. We thank Claire Robinson for the English revision of the manuscript.

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Authors and Affiliations

  1. UMS-IPSIT, US31 Inserm-UMS3679 CNRS, Plateforme d’Imagerie Cellulaire, Univ. Paris-Sud, Université Paris-Saclay, Faculté de Pharmacie, Tour E1, 5 Rue Jean-Baptiste Clément, 92296, Châtenay-Malabry, France

    Valérie Nicolas

  2. Laboratoire VEAC, Univ. Paris-Sud, Université Paris-Saclay, Faculté des Sciences, Bât. 360, Rue du Doyen André Guinier, 91405, Orsay, France

    Nathalie Oestreicher & Christian Vélot

  3. Pôle Risques MRSH-CNRS, Université de Caen, Esplanade de la Paix, 14032, Caen, France

    Nathalie Oestreicher & Christian Vélot

  4. CRIIGEN, 81 rue Monceau, 75008, Paris, France

    Christian Vélot

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  1. Valérie Nicolas
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  2. Nathalie Oestreicher
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Correspondence to Christian Vélot.

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Nicolas, V., Oestreicher, N. & Vélot, C. Multiple effects of a commercial Roundup® formulation on the soil filamentous fungus Aspergillus nidulans at low doses: evidence of an unexpected impact on energetic metabolism. Environ Sci Pollut Res 23, 14393–14404 (2016). https://doi.org/10.1007/s11356-016-6596-2

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