Honey bee genetics shape the strain-level structure of gut microbiota in social transmission

Abstract

Background Honey bee gut microbiota transmitted via social interactions are beneficial to the host health. Although the microbial community is relatively stable, individual variations and high strain-level diversity have been detected across honey bees. Although the bee gut microbiota structure is influenced by environmental factors, the heritability of the gut members and the contribution of the host genetics remains elusive. Considering bees within a colony are not readily genetically identical due to the polyandry of the queen, we hypothesize that the microbiota structure can be shaped by host genetics. Results We used shotgun metagenomics to simultaneously profile the microbiota and host genotypes of bees from hives of four different subspecies. Gut composition is more distant between genetically different bees at both phylotype- and “sequence-discrete population” levels. We then performed a successive passaging experiment within colonies of hybrid bees generated by artificial insemination, which revealed that the microbial composition dramatically shifts across batches of bees during the social transmission. Specifically, different strains from the phylotype of Snodgrassella alvi are preferentially selected by genetically varied hosts, and strains from different hosts show a remarkably biased distribution of single-nucleotide polymorphism in the Type IV pili loci. Genome-wide association analysis identified that the relative abundance of a cluster of Bifidobacterium strains is associated with the host glutamate receptor gene specifically expressed in the bee brain. Finally, mono-colonization of Bifidobacterium with a specific polysaccharide utilization locus impacts the alternative splicing of the gluR-B gene, which is associated with an increased GABA level in the brain. Conclusions Our results indicated that host genetics influence the bee gut composition and suggest a gut-brain connection implicated in the gut bacterial strain preference. Honey bees have been used extensively as a model organism for social behaviors, genetics, and the gut microbiome. Further identification of host genetic function as a shaping force of microbial structure will advance our understanding of the host-microbe interactions.

Significant compositional and functional variation reveals the patterns of gut microbiota evolution among the widespread Asian honeybee populations

“…In the western honeybee, host genetics influenced the gut microbe composition, where Bifidobacterium abundance was associated with the genotype of the host glutamate receptor (Wu et al, 2021). Different from Wu et al (2021), the complex background heterogeneity combined with a limited sample size might have masked apparent host genetic influence on gut bacteria at the local scale in our study, which may explain the weak signal reported in our GWAS analysis. However, our findings genuinely reflect the host genetic background and associated microbiota, which could not have been discovered without a broad scale sampling.…”

Strain-level profiling with picodroplet microfluidic cultivation reveals host-specific adaption of honeybee gut symbionts

“…2 A). We first estimated bacterial species abundance and strain-level genomic variation, including SNPs from shotgun metagenomic reads, using the MIDAS pipeline with a custom database for bee microbiome [ 35 ]. Then, we restored the bacterial genomes using genome-resolved metagenomic approaches based on the metagenomic assembly and clustering of contigs through the metagenomic binning procedure.…”

“…The species- and strain-level community profiling and gene content estimation were performed using the Metagenomic Intra-Species Diversity Analysis System (MIDAS) pipeline [ 34 ]. As described in our previous study [ 35 ], the custom database included genomes of pure isolates from the guts of A. mellifera , Apis cerana , Apis dorsata , and Bombus species. The relative abundance of species clusters was estimated by mapping quality-filtered reads to the database of phylogenetic marker genes using HS-BLASTN with the “run_midas.py species” module.…”

Geographical resistome profiling in the honeybee microbiome reveals resistance gene transfer conferred by mobilizable plasmids

“…To exclude the contigs without ARGs, we aligned the reads previously mapped to the ARGs in the MEGARes database (see above) to the assembled contigs with BLASTn, and only contigs possessing ARGs were applied for the taxonomy classification. The taxonomy of the assembled contigs containing ARGs was determined by comparing to the custom genomic database of both honey and bumble bee gut bacteria [ 29 ] using the two-way reciprocal best hit analysis.…”

“…Strains of the honeybee gut bacteria, Gilliamella apicola , Gilliamella apis , Bartonella apis , and Snodgrassella alvi , were isolated from the gut of A. mellifera [ 29 ]. The core gut bacteria of bee guts were obtained by plating the gut homogenates on Brain Heart Infusion (BHI; Oxoid, Basingstoke, UK)) or Columbia agar medium supplemented with 5% (vol/vol) defibrinated sheep blood (Solarbio, Beijing, China) at 35 °C under a CO 2 -enriched atmosphere (5%) for 2 days.…”