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Haemoproteomics of Bombus terrestris following pesticide exposure and interaction with Crithidia bombi

ABSTRACT: Pesticides pose a potential threat to bee health, especially in combination with other stressors, like parasites. However, pesticide risk assessment tests them in isolation from other stresses. We tested acute oral doses of three pesticides - glyphosate, Amistar and sulfoxaflor - on the bumblebee, Bombus terrestris, alongside the gut parasite Crithidia bombi. We found no impact of any pesticide on parasite intensity and no impact of sulfoxaflor or glyphosate on survival or weight change. Amistar caused weight loss and 19-41% mortality. Haemoproteome analysis showed various protein dysregulations. The major pathways dysregulated are those involved in insect defences and immune responses, with Amistar having the strongest impact on these. Our results show that while no response can be seen at a whole organism level, MALDI BeeTyping® can detect effects. Mass spectrometry analysis of bee haemolymph represent a pertinent tool to evaluate the stressor impacts on bee health, even at the individual scale.

INSTRUMENT(S): Q Exactive

ORGANISM(S): Crithidia Bombi Bombus Terrestris Terrestris

TISSUE(S): Haemolymphatic Fluid, Hemolymph

SUBMITTER: Karim Arafah

LAB HEAD: Dr. Philippe Bulet

PROVIDER: PXD039916 | Pride | 2023-02-09

REPOSITORIES: Pride

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Project description: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.

Project description:Pollinators are of crucial importance for maintaining biodiversity in ecosystems and for agriculture, including the Buff-tailed bumblebee Bombus terrestris. The health decline in these populations is thought to be linked to various abiotic and biotic stressors. In the hope of protecting these populations, deciphering their immune response in stress conditions represent a critical issue. To assess this metric, we analysed the bumblebee hemolymph, as a readout of the immune status. Here, we show in laboratory conditions that bacterial infections with two entomopathogenic strains and a well-recognised inducer of defence reactions in insects, impact the systemic immune response. Analysis of the hemolymph was carried out using a two-stage approach of mass spectrometry that combines MALDI molecular mass fingerprinting (MALDI MFP or MALDI-BeeTyping®) for its effectiveness in assessing the immune status of the bumblebee through a basic “blood” test and LC-ESI-MS/MS to measure the impact of our infectious models on the “haemoproteome”. By carrying out three different types of bacterial infections, we found that the bumblebee reacts in a specific way to bacterial attacks. Indeed, bacteria impact mortality and stimulate an immune response in infected individuals that is visible through changes in the molecular composition of their hemolymph. The characterisation and label-free quantification of proteins involved in specific signalling pathways in bumblebees by LC-ESI-MS/MS revealed differences in the protein expression between the non-experimentally infected and the infected bumblebees. Our results highlights differences in the molecular composition of their hemolymph to distinguish these different infections from non-experimentally infected bumblebees, and an alteration of pathways involved in (i) immunity and defences, (ii) the metabolism of carbohydrates (glycolysis), (iii) oxidative stress and (iv) amino acid biosynthesis. To conclude, we established bioinformatics models based on molecular markers reflecting the health status of these pollinators to enable diagnosis/prognosis at the population level in response to environmental stress.

Project description:<div>BACKGROUND: Epidemiological evidence suggests a link between pesticide exposure and the development of metabolic diseases. However, most experimental studies have evaluated the metabolic effects of pesticides using individual molecules, often at non-relevant doses or in combination with other risk factors such as high fat diets.<br></div><div>OBJECTIVES: We aimed to evaluate, in mice, the metabolic consequences of chronic dietary exposure to a pesticide mixture at non-toxic doses, relevant to consumers’ risk assessment.<br></div>METHODS: A mixture of six pesticides commonly used in France i.e. boscalid, captan, chlorpyrifos, thiofanate, thiacloprid, and ziram was incorporated in a standard chow diet, at doses exposing mice to the acceptable daily intake (ADI) of each pesticide. Wild-type (WT) and Constitutive Androstane Receptor knock-out (CAR-/-) C57Bl6/J male and female mice were exposed for 52 weeks. We assessed metabolic parameters (body-weight, food and water consumption, glucose tolerance, urinary metabolome) throughout the experiment. At the end of the experiment, we evaluated liver metabolism (histology, transcriptomics, metabolomics) and pesticide detoxification using LC/MS.<br>RESULTS: In males, pesticide exposure increased body weight and adiposity and induced hepatic steatosis and glucose intolerance. Exposed females exhibited fasted hyperglycaemia, hepatic oxidative stress and perturbations of gut microbiota-related urinary metabolites. The Constitutive Androstane Receptor is involved in the sexually dimorphic response to pesticide exposure.<br><div> CONCLUSIONS: We show for the first time the sexually dimorphic obesogen and diabetogen effects of a chronic dietary exposure <br>to a realistic mixture of pesticides, which are partially mediated through CAR. This raises questions about the relevance of ADI for <br>individual pesticides when present in a mixture.</div><div><br></div><div><b>Untargeted urine, plasma and liver NMR assay</b> protocols and data are reported in the current study <b>MTBLS602</b>.<br><br><b>Untargeted urine UPLC-MS assay</b> protocols and data associated to this study are reported in <a href="https://www.ebi.ac.uk/metabolights/MTBLS596"><b>MTBLS596</b></a>.<br></div><div><br></div>

Project description:<div>BACKGROUND: Epidemiological evidence suggests a link between pesticide exposure and the development of metabolic diseases. However, most experimental studies have evaluated the metabolic effects of pesticides using individual molecules, often at non relevant doses or in combination with other risk factors such as high fat diets.<br></div><div>OBJECTIVES: We aimed to evaluate, in mice, the metabolic consequences of chronic dietary exposure to a pesticide mixture at non-toxic doses, relevant to consumers’ risk assessment.<br></div> METHODS: A mixture of six pesticides commonly used in France i.e. boscalid, captan, chlorpyrifos, thiofanate, thiacloprid, and ziram was incorporated in a standard chow diet, at doses exposing mice to the acceptable daily intake (ADI) of each pesticide. Wild-type (WT) and Constitutive Androstane Receptor knock-out (CAR-/-) C57Bl6/J male and female mice were exposed for 52 weeks. We assessed metabolic parameters (body-weight, food and water consumption, glucose tolerance, urinary metabolome) throughout the experiment. At the end of the experiment, we evaluated liver metabolism (histology, transcriptomics, metabolomics) and pesticide detoxification using LC/MS.<br>RESULTS: In males, pesticide exposure increased body weight and adiposity and induced hepatic steatosis and glucose intolerance. Exposed females exhibited fasted hyperglycaemia, hepatic oxidative stress and perturbations of gut microbiota-related urinary metabolites. The Constitutive Androstane Receptor is involved in the sexually dimorphic response to pesticide exposure.<br><div> CONCLUSIONS: We show for the first time the sexually dimorphic obesogen and diabetogen effects of a chronic dietary exposure to a realistic mixture of pesticides, which are partially mediated through CAR. This raises questions about the relevance of ADI for individual pesticides when present in a mixture.</div><div><br></div><div><b>Untargeted urine UPLC-MS assay</b> protocols and data are reported in the current study <b>MTBLS596</b>.</div><div><br><b>Untargeted urine, plasma and liver NMR assay</b> protocols and data associated to this study are reported in <a href=https://www.ebi.ac.uk/metabolights/mtbls602><b>MTBLS602</b></a>.<br></div>

			Action	DRS
	EDAS_NSI_C171.msf	Msf
	EDAS_NSI_C171.raw	Raw
	EDAS_NSI_C174.msf	Msf
	EDAS_NSI_C174.raw	Raw
	EDAS_NSI_C180.msf	Msf

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Haemoproteomics of Bombus terrestris following pesticide exposure and interaction with Crithidia bombi

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