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Dietary Contamination with a Neonicotinoid (Clothianidin) Gradient Triggers Specific Dysbiosis Signatures of Microbiota Activity along the Honeybee (Apis mellifera) Digestive Tract.

ABSTRACT: Pesticides are increasing honeybee (Apis mellifera) death rates globally. Clothianidin neonicotinoid appears to impair the microbe-immunity axis. We conducted cage experiments on newly emerged bees that were 4-6 days old and used a 16S rRNA metataxonomic approach to measure the impact of three sublethal clothianidin concentrations (0.1, 1 and 10 ppb) on survival, sucrose syrup consumption and gut microbiota community structure. Exposure to clothianidin significantly increased mortality in the three concentrations compared to controls. Interestingly, the lowest clothianidin concentration was associated with the highest mortality, and the medium concentration with the highest food intake. Exposure to clothianidin induced significant variation in the taxonomic distribution of gut microbiota activity. Co-abundance network analysis revealed local dysbiosis signatures specific to each gut section (midgut, ileum and rectum) were driven by specific taxa. Our findings confirm that exposure to clothianidin triggers a reshuffling of beneficial strains and/or potentially pathogenic taxa within the gut, suggesting a honeybee's symbiotic defense systems' disruption, such as resistance to microbial colonization. This study highlights the role of weak transcriptional activity taxa in maintaining a stable honeybee gut microbiota. Finally, the early detection of gut dysbiosis in honeybees is a promising biomarker in hive management for assessing the impact exposure to sublethal xenobiotics.

SUBMITTER: El Khoury S

PROVIDER: S-EPMC8619528 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:The toxicity of pesticides used in agriculture towards non-targeted organisms and especially pollinators has recently drawn the attention from a broad scientific community. Increased honeybee mortality observed worldwide certainly contributes to this interest. The potential role of several neurotoxic insecticides in triggering or potentiating honeybee mortality was considered, in particular phenylpyrazoles and neonicotinoids, given that they are widely used and highly toxic for insects. Along with their ability to kill insects at lethal doses, they can compromise survival at sublethal doses by producing subtle deleterious effects. In this study, we compared the bee's locomotor ability, which is crucial for many tasks within the hive (e.g. cleaning brood cells, feeding larvae…), before and after an acute sublethal exposure to one insecticide belonging to the two insecticide classes, fipronil and thiamethoxam. Additionally, we examined the locomotor ability after exposure to pyrethroids, an older chemical insecticide class still widely used and known to be highly toxic to bees as well. Our study focused on young bees (day 1 after emergence) since (i) few studies are available on locomotion at this stage and (ii) in recent years, pesticides have been reported to accumulate in different hive matrices, where young bees undergo their early development. At sublethal doses (SLD48h, i.e. causing no mortality at 48 h), three pyrethroids, namely cypermethrin (2.5 ng/bee), tetramethrin (70 ng/bee), tau-fluvalinate (33 ng/bee) and the neonicotinoid thiamethoxam (3.8 ng/bee) caused a locomotor deficit in honeybees. While the SLD48h of fipronil (a phenylpyrazole, 0.5 ng/bee) had no measurable effect on locomotion, we observed high mortality several days after exposure, an effect that was not observed with the other insecticides. Although locomotor deficits observed in the sublethal range of pyrethroids and thiamethoxam would suggest deleterious effects in the field, the case of fipronil demonstrates that toxicity evaluation requires information on multiple endpoints (e.g. long term survival) to fully address pesticides risks for honeybees. Pyrethroid-induced locomotor deficits are discussed in light of recent advances regarding their mode of action on honeybee ion channels and current structure-function studies.

Dataset Information

Dietary Contamination with a Neonicotinoid (Clothianidin) Gradient Triggers Specific Dysbiosis Signatures of Microbiota Activity along the Honeybee (Apis mellifera) Digestive Tract.

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