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Set of watercolor beetles

Chemical poses serious threat to our ecosystems, new study shows. Report: Claire Robinson

Glyphosate has already been shown to negatively affect microorganisms in the gut of honeybees, making the bees more susceptible to various stress factors. And a recently published study showed that glyphosate and the glyphosate-based herbicide formulation known as MON 52276 inhibited the shikimate pathway, a metabolic pathway occurring in plants and many microorganisms, in the bacterial populations of the rat gut microbiome.
 
Now glyphosate has been shown to inhibit the symbiotic bacteria of the grain beetle and the shikimate pathway is once again involved, according to a new study by scientists from the Johannes Gutenberg University in Mainz (JGU), the Max Planck Institute for Chemical Ecology in Jena, and the National Institute of Advanced Industrial Science and Technology in Japan.
 
Damage to the shikimate pathway is important because saw-toothed grain beetles live in a symbiotic relationship with bacteria. Their bacterial partners provide important building blocks for the formation of the insect's exoskeleton, which protects the beetles from their enemies as well as from desiccation.
 
The researchers found that beetles exposed to glyphosate no longer receive the building blocks they need from the bacteria. And the researchers went on to show that many mutually beneficial bacteria associated with various different insect hosts were also glyphosate-sensitive, suggesting insects might be at risk of harm more generally via their bacterial partners and this could be contributing to the high level of insect decline currently taking place.
 
Glyphosate alone, rather than a glyphosate herbicide formulation (which has added toxic ingredients) was tested in the study.

Insects need microbial partners to survive

Organisms do not exist in isolation but in an intricate network of ecological interactions. These interactions must be kept in mind when judging the impact of human activities. Insects in particular benefit in diverse ways from microbial symbionts, mostly via supplemented nutrients and chemical defences. However, the benefits derived from such symbiotic associations may also make the insect more vulnerable. Insect hosts often become so reliant on their microbial partners that they can hardly survive alone. Without symbiosis, insects' development may be delayed or prevented, their susceptibility to natural enemies may be increased, their reproductive potential and competitiveness with members of the same species may be impaired, or they may die.

Glyphosate prevents symbiotic bacteria from providing building blocks for insect exoskeleton

Glyphosate is one of the most widely used pesticides in agriculture, despite increasing controversy about its harmful effects. It is supposed to selectively suppress the growth of plants by inhibiting the biosynthesis of aromatic amino acids via the shikimate pathway. Animals, on the other hand, do not encode the shikimate pathway, and thus have been claimed to be unharmed by glyphosate.
 
However, many animals engage in interactions with symbiotic microbes that rely on the shikimate pathway to produce amino acids required by these animals. Tobias Engl, one of the lead authors of the study, said, "An impact of glyphosate on animals via their essential bacterial partners that use or even specialize in the shikimate metabolic pathway seems obvious, once the interaction of both partners is understood."
 
Furthermore, mutually beneficial bacteria that interact with several types of herbivorous insects provide a core benefit: the aromatic amino acid tyrosine, which is needed for the biosynthesis of the insect exoskeleton (cuticle).
 
This dependence on symbiosis may render insect herbivores particularly vulnerable to glyphosate in agriculture, as the herbicide inhibits the shikimate pathway in their symbiotic bacteria. As a result, important amino acids needed for cuticle formation are missing.

Is dependence on their symbiotic partners the Achilles heel of insects?

In the new study, the scientists show that glyphosate negatively influences the symbiotic bacteria harboured by the saw-toothed grain beetle, Oryzaephilus surinamensis. Exposure to the herbicide completely abolished the mutual benefit that the symbiotic bacteria provide for the formation of the cuticle, an insect's primary protection against stresses, such as drought or predator attack.

While the grain beetle is viewed as a pest and therefore some may welcome glyphosate's damaging effect, the researchers see it as a model organism for insects in general, which also rely on their symbiotic bacterial partners. The researchers state that their findings paint "an alarming picture" and suggest that "glyphosate application holds a tremendous risk of severe ecological impacts". This is especially so "in light of recent declines in the number and diversity of insects".
 
The researchers sequenced the genome of the symbiont associated with O. surinamensis. The tiny symbiont genome (300 kbp) contains the genetic instruction for a metabolism specialised in the synthesis of aromatic amino acids via the shikimate pathway. Interestingly, the genome strongly resembles that of the bacterial partners of the palm weevil, which are also involved in cuticle formation, although these symbionts belong to a different group of bacteria.
 
"Finding a functionally equivalent symbiotic relationship that arose independently in two different bacteria phyla and distantly related beetle families highlights the importance of cuticle-supporting symbioses in beetles," said Julian Kiefer, the study's first author. The scientists tested the functional benefits for the host experimentally by supplementing the beetles' diet with aromatic amino acids, thus compensating for the elimination of their symbionts. Conversely, glyphosate exposure inhibited the establishment of the symbiotic bacteria throughout the beetle's development and completely abolished the mutual benefit for cuticle synthesis.

Glyphosate a general threat

Engl explained: "When we observed the detrimental impact of glyphosate exposure on this symbiotic association, we wondered whether glyphosate poses a general threat to insects that depend on their microbial partners." By using phylogenetic analyses, the authors demonstrate that many mutually beneficial bacteria associated with various different insect hosts indeed encode a glyphosate-sensitive enzyme in the shikimate pathway, suggesting that the susceptibility of its microbial symbionts to glyphosate represents an Achilles heel for an insect.
 
We are currently experiencing insect decline on a massive scale. Insect abundance is decreasing, as is insect diversity, not to mention the impact of the disappearance of bees, beetles and other insects at higher levels in the food chain. The new findings highlight the fact that the use of the herbicide glyphosate in agriculture endangers vital symbiotic relationships between insects and microorganisms and thus poses a serious threat to our ecosystems.


Main source of comment: Max-Planck Institute
https://www.mpg.de/16862163/0506-choe-a-beetle-s-achilles-heel-155371-x
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The new study:
Kiefer, J. S. T. et al., Inhibition of a nutritional endosymbiont by glyphosate abolishes mutualistic benefit on cuticle synthesis in Oryzaephilus surinamensis. Communications Biology 4, 11 May 2021
https://www.nature.com/articles/s42003-021-02057-6

Abstract

Glyphosate is widely used as a herbicide, but recent studies begin to reveal its detrimental side effects on animals by targeting the shikimate pathway of associated gut microorganisms. However, its impact on nutritional endosymbionts in insects remains poorly understood. Here, we sequenced the tiny, shikimate pathway encoding symbiont genome of the sawtoothed grain beetle Oryzaephilus surinamensis. Decreased titers of the aromatic amino acid tyrosine in symbiont-depleted beetles underscore the symbionts’ ability to synthesize prephenate as the precursor for host tyrosine synthesis and its importance for cuticle sclerotization and melanization. Glyphosate exposure inhibited symbiont establishment during host development and abolished the mutualistic benefit on cuticle synthesis in adults, which could be partially rescued by dietary tyrosine supplementation. Furthermore, phylogenetic analyses indicate that the shikimate pathways of many nutritional endosymbionts likewise contain a glyphosate sensitive 5-enolpyruvylshikimate-3-phosphate synthase. These findings highlight the importance of symbiont-mediated tyrosine supplementation for cuticle biosynthesis in insects, but also paint an alarming scenario regarding the use of glyphosate in light of recent declines in insect populations.