Glyphosate and its formulations Roundup Bioflow and RangerPro alter bacterial and fungal community composition in the rat caecum microbiome
The following article was published in Front Microbio (Frontiers in Microbiology), October 5, 2022. This is an open access journal publishing under the Creative Commons Attribution license (CC-BY). The work can be freely shared and adapted provided that appropriate credit is given and any changes specified.
This journal article is freely available online so we are publishing the abstract, part of the introduction, a few quoted highlights, and conclusions. Follow the DOI link to read and/or download the entire article at doi: 10.3389/fmicb.2022.888853
Authors: Robin Mesnage, Simona Panzacchi, Emma Bourne, Charles A. Mein, Melissa J. Perry, Jianzhong Hu, Jia Chen, Daniele Mandrioli, Fiorella Belpoggi, and Michael N. Antoniou
 Figure 1 Bacterial and Fungal diversity is altered in the gut microbiome of rat exposed to either glyphosate or its herbicide formulations Roundup Bioflow and RangerPro. |
Abstract
The potential health consequences of glyphosate-induced gut microbiome alterations have become a matter of intense debate. As part of a multifaceted study investigating toxicity, carcinogenicity and multigenerational effects of glyphosate and its commercial herbicide formulations, we assessed changes in bacterial and fungal populations in the caecum microbiota of rats exposed prenatally until adulthood (13 weeks after weaning) to three doses of glyphosate (0.5, 5, 50 mg/kg body weight/day), or to the formulated herbicide products Roundup Bioflow and RangerPro at the same glyphosate-equivalent doses. Caecum bacterial microbiota were evaluated by 16S rRNA sequencing whilst the fungal population was determined by ITS2 amplicon sequencing. Results showed that both fungal and bacterial diversity were affected by the Roundup formulations in a dose-dependent manner, whilst glyphosate alone significantly altered only bacterial diversity. At taxa level, a reduction in Bacteroidota abundance, marked by alterations in the levels of Alloprevotella, Prevotella and Prevotellaceae UCG-003, was concomitant to increased levels of Firmicutes (e.g., Romboutsia, Dubosiella, Eubacterium brachy group or Christensenellaceae) and Actinobacteria (e.g., Enterorhabdus, Adlercreutzia, or Asaccharobacter). Treponema and Mycoplasma also had their levels reduced by the pesticide treatments. Analysis of fungal composition indicated that the abundance of the rat gut commensal Ascomycota Kazachstania was reduced while the abundance of Gibberella, Penicillium, Claviceps, Cornuvesica, Candida, Trichoderma and Sarocladium were increased by exposure to the Roundup formulations, but not to glyphosate. Altogether, our data suggest that glyphosate and its Roundup RangerPro and Bioflow caused profound changes in caecum microbiome composition by affecting the fitness of major commensals, which in turn reduced competition and allowed opportunistic fungi to grow in the gut, in particular in animals exposed to the herbicide formulations. This further indicates that changes in gut microbiome composition might influence the long-term toxicity, carcinogenicity and multigenerational effects of glyphosate-based herbicides.
Keywords: microbiota (16S), mycobiome, glyphosate, toxicity, pesticides
Introduction:
Glyphosate is a broad-spectrum herbicide active ingredient and the most used pesticide worldwide. Glyphosate-based herbicides are used to control weeds in agricultural fields and urban environments, but also to desiccate crops shortly before harvest. The use of glyphosate-based herbicides such as Roundup has increased exponentially since their introduction at the end of the 1970s due to the wide-scale adoption of glyphosate tolerant genetically modified crops, especially in North and South America (Benbrook, 2016). It is estimated that about 700,000 tons of glyphosate are used worldwide annually (Maggi et al., 2019). Although the use of glyphosate is expected to further increase by 2025 (Maggi et al., 2019), its application is reaching a plateau in some countries due to the spread of glyphosate-resistant weed species (Heap, 2014). In addition, controversies surrounding the toxicity of glyphosate has led to bans or restrictions of glyphosate usage (Robinson et al., 2020).
Highlights:
1. Analysis of alterations in fungal composition at the genus level (Supplementary Table 2) indicated that the abundance of Kazachstania (Ascomycota) was reduced while the abundance of Gibberella, Penicillium, Claviceps, Cornuvesica, Candida, Trichoderma and Sarocladium were increased by the treatments with the two Roundup formulated products (Figure 4). Glyphosate had limited effects on the mycobiome. Overall, these observations further suggest that exposure to glyphosate and its formulations affects the abundance of major bacteria taxa, which in turn reduces competition and allows opportunistic fungi to grow in the gut of the exposed animals.
2. Starting treatment at a prenatal stage of development appears to be not only more representative of real-world exposure scenarios but is apparently able to reveal effects of glyphosate and Roundup formulations that are not detected when treatment is initiated in adult animals, which have more mature and stable gut microbial communities. The adult gut microbiome is relatively stable and resilient to environmental perturbations (Lozupone et al., 2012). In contrast, the developing gut microbiome in infants appears to be more sensitive to perturbations, which could durably impact health during adult life (Robertson et al., 2019).
3. However, the changes caused by glyphosate and the two formulated products are comparable but more severe with the formulations, suggesting that the surfactants may enhance the effects of glyphosate as they do in plants in order for glyphosate to act as an efficient weedkiller. Numerous studies have shown that POEA surfactants contribute to the toxicity of glyphosate weedkillers.
Conclusion:
In conclusion, we reveal that early life exposures starting prenatally to glyphosate or its formulated products Roundup Bioflow and RangerPro cause large changes in the composition of the rat gut microbiota. This indicates that alterations in gut microbiome composition will have to be taken into account in the next phases of the Global Glyphosate Study addressing long-term toxicity, carcinogenicity and multi-generational effects of glyphosate and glyphosate -based herbicide formulations.