Indirect Effects of the Herbicide Glyphosate on Plant, Animal and Human Health Through its Effects on Microbial Communities

Abstract

The herbicide glyphosate interferes with the shikimate pathway in plants and in major groups of microorganisms impeding the production of aromatic amino acids. Glyphosate application on plants results in a slow death, accelerated by reduced resistance to root pathogens. Extensive glyphosate use has resulted in increasing residues in soil and waterways. Although direct glyphosate effects on animals are limited, major concerns have arisen about indirect harmful side effects. In this paper, we focus on indirect effects of sublethal concentrations of glyphosate on plant, animal and human health due to shifts in microbial community compositions in successive habitats. Research results of glyphosate effects on microbial communities in soil, rhizosphere and animal guts have been contradictory due to the different integration levels studied. Most glyphosate studies have tested short-term treatment effects on microbial biomass or general community composition at higher taxonomic levels in soil, rhizosphere or animal intestinal tracts, and found little effect. More detailed studies showed reductions in specific genera or species as well as biological processes after glyphosate application. Plant growth promoting rhizobacteria and beneficial intestinal bacteria often are negatively affected, while pathogenic bacteria and fungi are enhanced. Such shifts in microbial community composition have been implicated in enhanced susceptibility of plants to Fusarium and Rhizoctonia, of birds and mammals to toxic Clostridium and Salmonella species, and of bees to Serratia and Deformed Wing Virus. In animals and humans, glyphosate exposure and concentrations in urine have been associated with intestinal diseases and neurological as well as endocrine problems, but cause-effect relationships need to be determined in more detail. Nevertheless, outbreaks of several animal and plant diseases have been related to glyphosate accumulation in the environment. Long-term glyphosate effects have been underreported, and new standards will be needed for residues in plant and animal products and the environment.

Does Glyphosate Affect the Human Microbiota?

“…Recently, we combined closely related bacterial species and different strains within species to identify changes in their sensitivity to glyphosate [ 7 ] under the microevolutionary perspective of Alignable Tight Genomic Clusters (ATGC) [ 22 ]. The study of the EPSPS enzyme showed that phylogenetic groups and bacterial lifestyle are key factors determining the intrinsic sensitivity to glyphosate, possibly resulting from thicker cell walls in addition to differences in EPSPS type [ 7 , 8 ]. Specifically, Firmicutes were significantly more resistant to glyphosate than the most sensitive Proteobacteria and Actinobacteria groups.…”

“…Moreover, a bacterial lifestyle was strongly associated with sensitivity, because facultative host-associated and parasitic bacteria are more sensitive to the herbicide than free-living bacteria. However, Van Bruggen et al showed that pathogens are generally less sensitive to glyphosate than host-associated and free-living bacteria, by analyzing literature data on minimal inhibitory concentrations for a large number of bacteria [ 8 ]. The microevolutionary analysis further revealed that bacteria may easily become resistant to glyphosate through small changes in the EPSPS active site in the short evolutionary time of ATGC with non-synonymous mutations and horizontal gene transfers [ 7 ].…”

“…Thus, glyphosate as a stress factor may reduce bacterial susceptibility, either as a stress response or via mutations and change the bacterial response to antibiotics [ 12 , 49 , 50 , 51 , 52 , 53 ]. In turn, the heavy use of antibiotics and other chemicals may lead to bacterial co- and cross-resistance to glyphosate and other antimicrobials [ 8 , 46 , 54 ]. Notably, however, sensitivity towards antimicrobial compounds depends on the given concentration; thus, it is necessary to empirically determine at which level of glyphosate, and GBH, bacteria are resistant or susceptible.…”

“…The popularization of glyphosate-based herbicides (GBHs) has been associated with an increased detection of glyphosate and its by-product aminomethylphosphonic acid (AMPA) in soil and water [ 3 , 4 , 5 ]. Here, we perceive the risk that glyphosate may modulate microbes that are essential to human well-being because the targeted shikimate pathway is present in many microbes [ 6 , 7 , 8 , 9 , 10 , 11 , 12 ]. The herbicide inactivates the central enzyme 5-enolpyruvylshikimate-3-phosphate synthase (EPSPS), an almos-universal enzyme in plants, fungi, and prokaryotes, for the synthesis of three aromatic amino acids [ 13 , 14 ].…”

Physiological and Metabolic Response of Arthrospira maxima to Organophosphates

“…Literature of the last ten years has focused on the medium and long-term effects of the persistence of organophosphates, revealing their toxicity and the serious impact on ecosystems of all environmental matrices (air, soil, rivers, sea) and consequently on the health of humans [ 1 , 2 ]. By contrast, related literature also reported conflicting results on the role of organophosphates in perturbing or modifying the activity and microbial composition in soil or water [ 3 , 4 , 5 ]. Glyphosate is one of the most used organophosphates in industrialized countries; it is a non-selective herbicide with broad-spectrum activity used to eliminate weeds in crops [ 6 ].…”