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

Abstract

Background The spread of antibiotic resistance genes (ARGs) has been of global concern as one of the greatest environmental threats. The gut microbiome of animals has been found to be a large reservoir of ARGs, which is also an indicator of the environmental antibiotic spectrum. The conserved microbiota makes the honeybee a tractable and confined ecosystem for studying the maintenance and transfer of ARGs across gut bacteria. Although it has been found that honeybee gut bacteria harbor diverse sets of ARGs, the influences of environmental variables and the mechanism driving their distribution remain unclear. Results We characterized the gut resistome of two closely related honeybee species, Apis cerana and Apis mellifera, domesticated in 14 geographic locations across China. The composition of the ARGs was more associated with host species rather than with geographical distribution, and A. mellifera had a higher content of ARGs in the gut. There was a moderate geographic pattern of resistome distribution, and several core ARG groups were found to be prevalent among A. cerana samples. These shared genes were mainly carried by the honeybee-specific gut members Gilliamella and Snodgrassella. Transferrable ARGs were frequently detected in honeybee guts, and the load was much higher in A. mellifera samples. Genomic loci of the bee gut symbionts containing a streptomycin resistance gene cluster were nearly identical to those of the broad-host-range IncQ plasmid, a proficient DNA delivery system in the environment. By in vitro conjugation experiments, we confirmed that the mobilizable plasmids could be transferred between honeybee gut symbionts by conjugation. Moreover, “satellite plasmids” with fragmented genes were identified in the integrated regions of different symbionts from multiple areas. Conclusions Our study illustrates that the gut microbiota of different honeybee hosts varied in their antibiotic resistance structure, highlighting the role of the bee microbiome as a potential bioindicator and disseminator of antibiotic resistance. The difference in domestication history is highly influential in the structuring of the bee gut resistome. Notably, the evolution of plasmid-mediated antibiotic resistance is likely to promote the probability of its persistence and dissemination.

Experimental inheritance of antibiotic acquired dysbiosis affects host phenotypes across generations

“…This is consistent with other studies that found effects of antibiotics ( Raymann et al, 2018 ) and other pesticides ( Cuesta-Maté et al, 2021 ) vary across bee gut bacterial species and strains. These data together with the increase in resistance genes in antibiotic exposed bee microbiomes ( Tian et al, 2012 ; Sun et al, 2022 ) indicate adaptation to chemical selection factors.…”

Comparing the taxonomic and functional profiles of gut microbiota from three pig breeds by metagenomic sequencing

“…The host genetics are consider as one important factor that could influence gut microbial diversity (Pajarillo et al, 2015;Sun et al, 2022), genetically related individuals tend to have more similar gut microbial composition than unrelated individuals (Campbell et al, 2012;Hildebrand et al, 2013). In order to explore the influence of host genetics on gut microbial community, we selected three pig breeds raised in the same environment as the subjects.…”

“…The inappropriate use of antibiotics can cause imbalance of gut microbiota, and induce an increased antibiotic resistance in this organisms (Guo et al, 2021). In addition, the host genetics are also a crucial determinant, it was widely reported that the microbial communities have a certain degree of breed specificity (Pajarillo et al, 2015;Sun et al, 2022).…”

Dysregulation of gut health in zebrafish by differentially charged nanoplastic exposure: an integrated analysis of histopathology, immunology, and microbial informatics

“…The V3 region of the 16S rRNA gene was amplified using the primer P2(5′ATTACGAGGAGCAG3′) through the ABI GeneAmp® 9700. 30 An Illumina MiSeq was used for high-throughput sequencing of 16S rRNA genes at Shanghai Majorbio Co., Ltd. PE reads obtained by Miseq sequencing were spliced according to the overlap relationship, and the sequence quality was controlled and filtered at the same time. OTU (operational taxonomic units) cluster analysis and species taxonomy analysis were carried out.…”