Dataset Information

The Gut-Brain-Microbiome Axis in Bumble Bees.

ABSTRACT: The brain-gut-microbiome axis is an emerging area of study, particularly in vertebrate systems. Existing evidence suggests that gut microbes can influence basic physiological functions and that perturbations to the gut microbiome can have deleterious effects on cognition and lead to neurodevelopmental disorders. While this relationship has been extensively studied in vertebrate systems, little is known about this relationship in insects. We hypothesized that because of its importance in bee health, the gut microbiota influences learning and memory in adult bumble bees. As an initial test of whether there is a brain-gut-microbiome axis in bumble bees, we reared microbe-inoculated and microbe-depleted bees from commercial Bombus impatiens colonies. We then conditioned experimental bees to associate a sucrose reward with a color and tested their ability to learn and remember the rewarding color. We found no difference between microbe-inoculated and microbe-depleted bumble bees in performance during the behavioral assay. While these results suggest that the brain-gut-microbiome axis is not evident in Bombus impatiens, future studies with different invertebrate systems are needed to further investigate this phenomenon.

SUBMITTER: Leger L

PROVIDER: S-EPMC7469151 | biostudies-literature | 2020 Aug

REPOSITORIES: biostudies-literature

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The Gut-Brain-Microbiome Axis in Bumble Bees.

Leger Laura L McFrederick Quinn S QS

Insects 20200810 8

The brain-gut-microbiome axis is an emerging area of study, particularly in vertebrate systems. Existing evidence suggests that gut microbes can influence basic physiological functions and that perturbations to the gut microbiome can have deleterious effects on cognition and lead to neurodevelopmental disorders. While this relationship has been extensively studied in vertebrate systems, little is known about this relationship in insects. We hypothesized that because of its importance in bee heal ...[more]

PMID: 32785118

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Project description:Eusocial corbiculate bees, including bumble bees and honey bees, maintain a socially transmitted core gut microbiome that contributes to digestion and pathogen defense. In contrast, solitary bees, which have fewer opportunities for direct interhost transmission, typically have less consistent microbiomes dominated by bacteria associated with pollen and food reserves. Carpenter bees (genus Xylocopa) are long-lived bees that are not eusocial but that often live in shared nesting sites. We characterized gut microbiomes for Xylocopa micans, X. mexicanorum, X. tabaniformis parkinsoniae, and X. virginica and for five solitary bee species from other genera (Andrena, Habropoda, Megachile, and Svastra), sampled in the same localities in central Texas. Unexpectedly, all four Xylocopa species had microbiomes dominated by bacterial lineages previously known only from social bees or other insect groups. Microbiomes were similar across three Xylocopa species and included lineages in the families Bifidobacteriaceae, Orbaceae, Lactobacillaceae, Pseudomonadaceae, and Enterobacteriaceae. In contrast, X. virginica had a distinct microbiome dominated by the genus Bombilactobacillus, a group abundant in guts of eusocial bees. Phylogenetic analyses support a past transfer of bacterial lineages into Xylocopa from bumble bees or honey bees. Gut microbiome compositions of Xylocopa species were distinct from those of other co-occurring solitary bees that had variable gut microbiomes dominated by bacteria from environmental sources. IMPORTANCE Gut microbiomes from social bees, such as honey bees and bumble bees, are conserved and consist of host-restricted bacteria that are transmitted among sterile female workers within a colony and that are important to the health of these key insect pollinators. In contrast, solitary bee species typically have more erratic, environmentally acquired microbiomes. Carpenter bees (genus Xylocopa) can be solitary as they lack a worker caste, and each female can excavate nests and raise offspring alone, although females are often social share nests at least in some species. This study showed that the gut microbiomes of four Xylocopa species have distinctive and consistent compositions and are dominated by bacterial lineages previously known from honey bees and bumble bees. Thus, eusociality is not required for bees to maintain a specialized, host-restricted gut microbiome. These findings suggest that gut bacteria are transmitted at shared nesting sites and that they play a role in host ecology.

Project description:Recent declines in bumble bee populations are of great concern and have prompted critical evaluations of the role of pathogen introductions and host resistance in bee health. One factor that may influence host resilience when facing infection is the gut microbiota. Previous experiments with Bombus terrestris, a European bumble bee, showed that the gut microbiota can protect against Crithidia bombi, a widespread trypanosomatid parasite of bumble bees. However, the particular characteristics of the microbiome responsible for this protective effect have thus far eluded identification. Using wild and commercially sourced Bombus impatiens, an important North American pollinator, we conducted cross-wise microbiota transplants to naive hosts of both backgrounds and challenged them with a Crithidia parasite. As with B. terrestris, we find that microbiota-dependent protection against Crithidia operates in B. impatiens Lower Crithidia infection loads were experimentally associated with high microbiome diversity, large gut bacterial populations, and the presence of Apibacter, Lactobacillus Firm-5, and Gilliamella spp. in the gut community. These results indicate that even subtle differences between gut community structures can have a significant impact on a microbiome's ability to defend against parasite infections.IMPORTANCE Many wild bumble bee populations are under threat due to human activity, including through the introduction of pathogens via commercially raised bees. Recently, it was found that the bumble bee gut microbiota can help defend against a common parasite, Crithidia bombi, but the particular factors contributing to this protection are unknown. Using both wild and commercially raised bees, we conducted microbiota transplants to show that microbiome diversity, total gut bacterial load, and the presence of certain core members of the microbiota may all impact bee susceptibility to Crithidia infection. Bee origin (genetic background) was also a factor. Finally, by examining this phenomenon in a previously uninvestigated bee species, our study demonstrates that microbiome-mediated resistance to Crithidia is conserved across multiple bumble bee species. These findings highlight how intricate interactions between hosts, microbiomes, and parasites can have wide-ranging consequences for the health of ecologically important species.

Dataset Information

The Gut-Brain-Microbiome Axis in Bumble Bees.

Publications

The Gut-Brain-Microbiome Axis in Bumble Bees.

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