Honeybee gut microbiota modulates host behaviors and neurological processes

Abstract

Honeybee is a highly social insect with a reach behavioral repertoire and is a versatile model for neurobiological research. The honeybee gut microbiota is composed of a limited number of bacterial phylotypes that play an important role in host health. However, it remains unclear whether the microbiota can shape brain profiles and behaviors. Here, we revealed that the gut microbiota is requisite for the olfactory learning and memory ability of honeybees and alters the level of neurotransmitters in the brain. Transcriptomic and proteomic analysis showed distinctive gene expression and protein signatures for gnotobiotic bees associated with different gut bacteria. Specifically, genes related to olfactory functions and labor division are most upregulated. Moreover, differentially spliced genes in the brains of colonized bees largely overlapped with the datasets for human autism. The circulating metabolome profiles identified that different gut species regulated specific module of metabolites in the host hemolymph. Most altered metabolites are involved in the amino acid and glycerophospholipid metabolism pathways for the production of neuroactive compounds. Finally, antibiotic treatment disturbed the gut community and the nursing behavior of worker bees under field conditions. The brain transcripts and gut metabolism was also greatly interfered in treated bees. Collectively, we demonstrate that the gut microbiota regulates honeybee behaviors, brain gene transcription, and the circulating metabolism. Our findings highlight the contributions of honeybee gut microbes in the neurological processes with striking parallels to those found in other animals, thus providing a promising model to understand the host-microbe interactions via the gut-brain axis.

Inflammatory bowel disease-associated Escherichia coli strain LF82 in the damage of gut and cognition of honeybees

“…Associative olfactory learning and memory experiments were performed according to the standard PER protocols ( Menzel, 2009 ; Matsumoto et al., 2012 ; Zhang et al, 2021 ) with modifications as follows ( Figure 1B ): 25 bees were taken from each group 5 days after the E. coli exposure. Bees were tied into a sectioned hollow metal tube and starved for 2 h by removing foods.…”

Upper-limit agricultural dietary exposure to streptomycin in the laboratory reduces learning and foraging in bumblebees

“…It is well established that microbes play a role on insect behaviour [60] and that microbial depletion via antibiotics can lead to behavioural changes in animals [61]. In honeybees, antibiotic exposure can impair individual olfactory learning, potentially driven by gut microbial depletion [62], and antibiotic applications within hives can delay the onset of foraging in workers [13]. It is thus plausible that disrupting the gut–brain axis led to learning delays (i.e.…”

“…The impact on bumblebee survival, however, depends on the antibiotic type and concentration [10,11]. Recent evidence suggests that exposure to high antibiotic doses can affect honeybee olfactory learning [12] and delay the onset of foraging in honeybee colonies [13], but much remains unknown about how antibiotics might impact other modes of bee learning, especially when given at the upper limit concentrations applied to crops.…”

“…For example, microbe-free flies ( Drosophila melanogaster ) take longer to associate an aversive reward with a stimulus relative to control flies with a gut microbial community [25]. Germ-free honeybees ( A. mellifera ) are less likely to display the proboscis-extension reflex when exposed to low-concentration sucrose solutions [26] and to associate odors with rewards [12], compared to bees with a normal microbiome. The abundance of a core gut microbial taxon ( Lactobacillus Firm-5 ) is also positively correlated with bumblebee memory of rewarding flowers [27].…”

Classic Hoarding Cages Increase Gut Bacterial Abundance and Reduce the Individual Immune Response of Honey Bee (Apis mellifera) Workers

“…The honey bee gut bacterial community, commonly referred to as the gut microbiome, contributes substantially to honey bee health and fitness ( Raymann and Moran 2018 ). Due to the highly conserved nature of the honey bee gut microbiome, as well as the global importance of honey bees as managed pollinators, significant efforts have been made to understand how the honey bee gut bacterial community interacts with its host and the environment ( Motta et al 2018 , Zheng et al 2018 , Castelli et al 2020 , Zhang et al 2020 ).…”