Research Article: Glyphosate, but not its metabolite AMPA, alters the honeybee gut microbiota

Date Published: April 16, 2019

Publisher: Public Library of Science

Author(s): Nicolas Blot, Loïs Veillat, Régis Rouzé, Hélène Delatte, Olav Rueppell.


The honeybee (Apis mellifera) has to cope with multiple environmental stressors, especially pesticides. Among those, the herbicide glyphosate and its main metabolite, the aminomethylphosphonic acid (AMPA), are among the most abundant and ubiquitous contaminant in the environment. Through the foraging and storing of contaminated resources, honeybees are exposed to these xenobiotics. As ingested glyphosate and AMPA are directly in contact with the honeybee gut microbiota, we used quantitative PCR to test whether they could induce significant changes in the relative abundance of the major gut bacterial taxa. Glyphosate induced a strong decrease in Snodgrassella alvi, a partial decrease of a Gilliamella apicola and an increase in Lactobacillus spp. abundances. In vitro, glyphosate reduced the growth of S. alvi and G. apicola but not Lactobacillus kunkeei. Although being no bee killer, we confirmed that glyphosate can have sublethal effects on the honeybee microbiota. To test whether such imbalanced microbiota could favor pathogen development, honeybees were exposed to glyphosate and to spores of the intestinal parasite Nosema ceranae. Glyphosate did not significantly enhance the effect of the parasite infection. Concerning AMPA, while it could reduce the growth of G. apicola in vitro, it did not induce any significant change in the honeybee microbiota, suggesting that glyphosate is the active component modifying the gut communities.

Partial Text

Glyphosate, or N-(phosphonomethyl)glycine, is as a broad-spectrum herbicide used for weed control. It blocks the plant growth by inhibiting the 5-enolpyruvylshikimate-3-phosphate synthase (EPSPS), an enzyme of the shikimate pathway involved in the synthesis of aromatic metabolites, including aromatic amino acids [1,2]. The EPSPS is present in plants but also in bacteria and fungi, but not in metazoans. Glyphosate is the most sprayed herbicide worldwide, especially under commercial formulations, the best known being Roundup. The frequency and intensity of glyphosate application as well as the surface of treated croplands have been growing constantly, especially since the marketing of Genetically Engineered Herbicide-Tolerant (GE-HT) crops. The wide use of the herbicide has for consequence the contamination of the environment by glyphosate and its metabolites, the most abundant being the aminomethylphosphonic acid (AMPA). AMPA is mainly produced from glyphosate metabolization by soil and saprophyte microorganisms and by second generation of GE-HT plants, but also from other human activities [3–5]. AMPA is more persistent than glyphosate in the environment. Glyphosate and AMPA can be found in all treated plant products but also in non-target plants, in the soil, in surface and groundwaters and even in the atmosphere [2,3]. Since glyphosate and AMPA contaminate water and plant matrices, they can be ingested by animal consumers. For instance, by foraging contaminated pollen, nectar and water, pollinators are exposed to glyphosate and its metabolites.

Interior overwintering honeybee workers were exposed to 1.5 mM of glyphosate in their feeding ad. lib., to spores of the parasite N. ceranae, or to both stressors. To verify the effect of glyphosate on the microbiota, a second experiment was performed on summer honeybees that were chronically exposed to 1.5 mM and 7.5 mM of glyphosate, of AMPA and of stoichiometric mixtures of both xenobiotics.

The present study confirmed the work of Motta et al. [31] by showing that glyphosate, although not lethal for the honeybee, can alter its gut microbiota. In relative abundance, a strong decrease in of S. alvi and an increase in Lactobacillus spp. were observed in response to glyphosate (Fig 1), which was consistent with the data of Motta et al. [31] in newly emerged and interior bees. In contrast, opposite results were observed on G. apicola. In absolute abundance, Motta et al. [31] showed that glyphosate induced a reduction in the total bacterial content of the honeybee gut microbiota, as well as a decrease in S. alvi, Lactobacillus spp. and Bifidobacterium spp..

In the context of honeybee population decline, where combinations of environmental contaminants are suspected, the weakening of honeybee health through the exposure to xenobiotics of low toxicity may be of importance. Glyphosate has sublethal effects on the honeybee gut microbiota, changing the abundance of major bacterial taxa, especially by affecting the growth of S. alvi. The consequences of such microbial disturbance are unclear: is the honeybee able to cope with glyphosate and preserve the gut homeostasis or will future data demonstrate that this changes are linked with a functional dysbiosis?