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Investigating the effects of glyphosate on the bumblebee proteome and microbiota

ABSTRACT: Glyphosate is one of the most widely used herbicides globally. It acts by inhibiting an enzyme in an aromatic amino synthesis pathway specific to plants and microbes, leading to view that glyphosate poses no risk to other organisms. However, there is growing concern that glyphosate is associated with detrimental health effects in humans, and an ever-increasing body of evidence suggests that glyphosate affects other animals including pollinating insects such as bees. Although pesticides have long been considered a contributing factor in the decline of wild bee populations most research on bees has focussed on demonstrating and understanding the effects (particularly sublethal ones) of insecticides. To assess whether glyphosate poses a potential risk to bees we characterised the changes in survival, behaviour, digestive tract proteome and microbiome in the bumblebee Bombus terrestris after chronic exposure to field relevant doses of glyphosate alone and as part of the commercially available product RoundUp Optima+®. Regardless of source, changes in response to herbicide exposure in important cellular and physiological processes in the digestive tract of B. terrestris were observed, with the abundances of proteins associated with oxidative stress regulation, metabolism, cellular adhesion, the extracellular matrix, and various signalling pathways being altered. Interestingly, endocytosis, oxidative phosphorylation, the TCA cycle, and carbohydrate, lipid, and amino acid metabolism were differentially altered depending on whether the exposure source was glyphosate AI or RoundUp Optima+®. In addition, RoundUp Optima+®, but not the active ingredient glyphosate, impacted fungal diversity in the digestive tract microbiota. Our research provides new insights into the potential mode of action and consequences of glyphosate exposure at the molecular and cellular levels in bumblebees and highlights issues with current regulatory measures involving commercial formulations of pesticides where the impact of the co-formulants on non-target organisms are generally overlooked.

INSTRUMENT(S): Q Exactive HF

ORGANISM(S): Apis Mellifera (honeybee)

SUBMITTER: James Carolan

LAB HEAD: Jim Carolan

PROVIDER: PXD036578 | Pride | 2023-07-01

REPOSITORIES: Pride

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			Action	DRS
	Bter_Chr_Gut_ComFor_1.raw	Raw
	Bter_Chr_Gut_ComFor_2.raw	Raw
	Bter_Chr_Gut_ComFor_3.raw	Raw
	Bter_Chr_Gut_ComFor_4.raw	Raw
	Bter_Chr_Gut_Cont_1.raw	Raw

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Project description:As a matter of fact, honeybees are vital for the pollination of more than 80 crops of agricultural interest. However, population decline has become an important global issue causing significant concerns among agricultural experts and the broader public. For this, parasites are known to be the major culprits responsible for the losses of millions of honeybee colonies so far. Among these parasites, Varroa destructor has been identified as a major cause for global losses in Western honeybee (Apis mellifera) colonies. Hygienic behavior (HB), on the other hand, is a collective response by adult honeybees to defend against parasites and diseases that is known to involve in resistance towards Varroosis. Even with the efforts made to elucidate the molecular mechanism underlying HB, it is still not understood. In our study, we have studied the proteomic correlates to HB using a honeybee line (selected for Varroa-specific HB for over a decade in Germany). We sampled individual worker bees from this line that showed HB after closer infrared video observations and compared the proteomes of their mushroom bodies and antennae with those of workers that came from the same set of colonies but didn't show the behaviour. Furthermore, we compared the pupal hemolymph for worker bees of the selected HB line and a control line using state-of-the art techniques of proteomics. We identified a total of 8609 proteins (covered >55% of the honeybee proteome) from these three honeybee tissues. This is the most comprehensive proteomic study of the honeybee HB to date, and the first to focus on individual bees expressing Varroa-specific HB. These results have significantly advanced our knowledge on the biology underlining HB to a new level. The uniquely found functional classes and pathways by the proteins identified in each tissue suggest that hygienic bees have shaped distinct proteome settings to underpin the HB. Moreover, during analysis of pupal hemolymph proteome, the HB-line has adapted a unique strategy to boost an individual and social immunity and drove pupal organogenesis via energy metabolism and protein biosynthesis. Moreover, in the mushroom bodies of different HB phenotypic worker bees, the hygienic bees have enhanced their neuronal sensitivity to promote the execution of HB by activation of synaptic vesicles and calcium channel activities. Moreover, in the antennae of two HB phenotypic worker bees, the hygienic bees have demonstrated strengthening of their sensitivity associated with olfactory senses and signal transmissions, which is important to input a strong signal to the mushroom bodies and initiate HB. In conclusion, our novel findings have significantly extended our understandings of the molecular mechanisms that underline the HB to combat Varroa infestation. Furthermore, we identified a wide array of novel markers that are useful for accelerating marker associated selection of HB to aid in the natural resistance to a parasite blamed for a global decline in honeybee health.

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Investigating the effects of glyphosate on the bumblebee proteome and microbiota

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